The pelagic environment covers approximately 70% of the
planet's total surface (139,768,409 sq mi or 362 million sq km)
with an average depth of 12,238 ft (3,730 m), and thus occupies a volume
of approximately 1,350 million [km.sup.3], making it the largest
environment on Earth.

From plankton to nekton

In a terrestrial ecosystem, the most important primary producers
occupy fixed positions and many animals move in only two dimensions. The
entire depth of the sea's water layer is inhabited, from the
surface to the seafloor, and even within the sediment. Some of its
inhabitants are suspended in the water, either swimming or drifting, and
are called pelagic organisms. These organisms form part of ecosystems
that are also called pelagic or, in other words, belonging to the open
or high seas. These ecosystems show a significant degree of
indeterminacy in the position of the individuals that interact in them
and there is a considerable gradient of possibilities, ranging from
those that seem to occur at random, such as interactions between
non-mobile planktonic organisms, to ones showing greater determination,
such as the pursuit of a mobile alga by a swimming animal.

The benthic organisms and ecosystems, which form the benthos, are
distinguished from pelagic ones as they are close to or associated with
the ocean bottom, whether rocky or sediments. This distinction is highly
artificial, given that many pelagic species deposit their eggs on the
bottom and many benthic species release their eggs and thus--together
with their larvae--form part of the plankton until a relatively advanced
stage of their metamorphosis. Furthermore, many pelagic organisms
interact with the seafloor and many benthic organisms leave the
substrate and make regular incursions into the water column. In
practice, however, there is agreement that pelagic species are those
whose adult forms normally live above the seafloor, within the water
column.

Pelagic organisms are subject to the general properties of the
marine environment: its fluidity and instability; the easy conduction of
dissolved materials, including nutrients and externally diffused active
substances (pheromones); and the propagation of compressional (pressure)
waves. These organisms also experience turbulent movements, superimposed
on a more regular and persistent circulation and stratification effects,
caused basically by the absorption of solar radiation. The raised
specific heat capacity of water and its movement mean that local
temperature differences are not as marked as on the surface of the
continents. It should be remembered that raising the temperature by
10[degrees]C roughly doubles the rate of most biochemical reactions (for
example, respiration, in a negative sense), while photosynthesis (in a
positive sense) is much less affected. As a general conclusion, lower
temperatures favor relatively higher net production, as long as the
water does not freeze, something that only happens on a very local
scale.

A question of size

Pelagic organisms come in all sizes. Some of them could more
appropriately be called semi-organisms, such as viruses, many of which
have been found in ocean water in great numbers, attaining
concentrations of 104 to 107 per ml. Bacteria are also widely
distributed, although most are not very active. If they were, they would
use a lot of organic nutrients and deplete the oxygen in the masses of
deep water. Large whales are at the opposite end of the scale of size.
The blue whale (Balaenoptera musculus)--which can reach 108 ft (33 m) in
length, 130 tons in weight, and whose speed ranges from 7-23 mph (6-20
knots)--is surely the largest animal that has ever existed on this
planet, the original Leviathan.

The range in size thus covers nine orders of magnitude. The name
plankton is given to the essentially passive components of this world in
suspension, a group whose limits have never been rigorously defined,
although one criterion is that they are always at the mercy of the water
movements. In short, plankton, as its etymological derivation suggests,
drifts. Within the pelagic environment, plankton is distinguished from
nekton, free-swimming animals that move at will in their environment, by
its obvious limitations.

Plankton for study was first collected using fine nets. It seems
that the first scientific samples were made by Vaughan Thomas
(1779-1847) in the Irish Sea (1828) and Johannes Muller (1801-1858) in
the Bay of Heligoland (1844). Plankton nets or filters were for a long
time made from the same silk nets that were used for sieving flour, and
so it was industrial considerations linked to the quality of the flour,
rather than strictly scientific ones, that determined historically the
distinctions between different groups of plankton. The smaller plankton,
the microplankton, that account for much of the mass of the autotrophic
plankton, was retained by the finest nets used, with a theoretical pore
size of 40 [micro]m.

The scientific community soon realized that even smaller organisms
were passing through the mesh of the nets, and scientists began to add
fixing and preserving agents to the water so the organisms were killed
and preserved virtually without deformation. The sedimented, dead
plankton was examined using a microscope with a special apparatus that
allowed the plankton to be viewed and counted from below (the Utermohl
or inverted microscope). This led to the creation of the additional
category of nanoplankton. Techniques for fixing the materials in the
best conditions for observation, as well as collection techniques, have
improved. Most fixatives have been suggested for some specific purpose,
but often present certain disadvantages. For a long time the agents used
were hot corrosive sublimate (mercuric chloride, HgCl2) or formalin.
Nowadays, sedimented plankton is widely studied using a solution of
iodine, and there are many very effective fixatives for specific
purposes.

Mechanical devices are now available with optical or
electromagnetic detectors that count the successive particles that pass
through a narrow orifice and divide them into categories, originally on
the basis of size and now also according to their fluorescence
properties. The final category, the picoplankton or ultraplankton, was
defined when the use of fluorescence or stains revealed the smallest
organisms, such as heterotrophic bacteria, cyanobacteria, and other
autotrophic bacteria. These distinctions and nomenclature are only worth
retaining so long as they are still useful. This question is of
historical interest because it shows how the importance attached to the
different groups has changed as ever smaller organisms were identified.

1.2 The movements of pelagic organisms

Drifting in the water or moving at will may, from a certain size
upwards, depend on the relative power attained by their organs of
movement at the end point culmination of a particular evolutionary
trend. A large jellyfish and an eastern Atlantic scad (Trachurus
trachurus) are similar in size, but different enough for some sort of
comparison to be made. Drifting or independent movement also depends on
the local water movements, and on whether there are important currents
with peripheral eddies, or whether the range of turbulence is restricted
to minor fluctuations without any clear prevailing direction. These
factors largely depend on the arrangement of the large water masses due
to movements of the liquid, down to the smallest scales.

Moving at will or drifting

Superimposed on the more or less regular turbulent agitation of the
medium, the trajectory followed by each individual can be considered as
an example of a "random walk." This is basically the result of
breaking a trajectory of a hybrid nature down into its basic steps. They
are sometimes partly determined by the organism's own
movement--down to nil--but are always partly determined by the influence
of the complex range of different forms of turbulence, ranging from
agitation to the circulation of the water. In more
"scientific" terms, any part of the trajectory can be
described so that the distance traveled, L, between its starting point
and its finishing point, expressed in the number of elemental steps, N,
is equal to a (reasonably small) number of elemental steps, N, raised to
an appropriate power between 0 and 1; thus L = [N.sup.k] (where 0 < k
< 1). In three dimensions, k may have three components, corresponding
to the x, y, and z coordinates ([k.sup.2] = [k.sup.2.sub.x] +
[k.sup.2.sub.y] + [k.sup.2.sub.z]). The vertical component [k.sub.z] is
probably the most determinant of these, and the most important from the
point of view of biology and evolution. This vertical component is
perceived everywhere, and vertical migration may occur wherever there is
a light gradient, even in water showing isotropic turbulence, not to
mention the perception of the direction of gravity. These trajectories
will also be influenced by the presence of other organisms of the same
or different species, which will be perceived either as a gradient of
attractive or repellent substances or as mechanical deformations in the
liquid. Natural selection may have acted on the generation of these
gradients, introducing factors that disorientate or confuse potential
predators. The question of the distinction between plankton and nekton
leads, if one wishes, to comparing the size and locomotor capacity of
each organism with some of the small-scale mechanical properties of
water, such as those seen in viscosity and in the range of turbulence
effects. An organism's autonomous capacity for movement depends on
its size, and in small organisms, on its degree of adherence to the
immediate strata of water. The properties of the contact between liquid
and solid are not only important in locomotion but also in the exchange
of fluids and the effectiveness of organs that mechanically filter food
particles.

The Reynolds number ([R.sub.e] = rVL/[micro]) is a good guide to
how "planktonic" an organism is. This is a dimensionless
number combining a measurement, L, considered as a characteristic of the
organism (such as its largest dimension), multiplied by its velocity, V,
with respect to the water (almost zero in passive organisms), and where
r is density and [micro] is the kinetic viscosity of the water,
expressed in poises (1 poise is equal to 10-1 N s m-2). The Reynolds
number is much less than 1 for a phytoplankton cell that sinks slowly.
Values up to 200 are found in laminar flows, while Reynolds numbers
greater than 2,000 are found where flow is clearly turbulent. If it is
500,000 or more, the organism is a large fish. This parameter thus
allows us to distinguish between different situations: plankton proper,
which shows greater adhesion to the water and is its slave, to such an
extent that the strata in contact with small organisms are renewed only
with difficulty and always by sliding; small active swimmers, such as
dinophytes and the nauplius larvae of copepods; and the true nekton. The
higher the Reynolds number, the more noticeable the series of eddies and
perturbations the organism leaves behind it that can serve--to its
detriment--as a guide or track for predators. The use of different
mechanical methods for dealing with the surrounding fluid is thought to
be of defensive importance because they are an attempt to throw
predators "off track" by reducing eddies, or by making them
deviate, thereby deceiving the predator.

Neither plankton or nekton

The Sargasso Sea houses a special community, an example of what
botanists call pleuston (creatures that are neither planktonic nor
nektonic), that consists of free individuals of at least two species of
Sargassum of Atlantic-American origin. These algae continue growing
close to the surface at the center of the North Atlantic anticyclonic
gyre, thanks to the buoyancy of their air bladders. A more complex kind
of life with interesting, or even spectacular, biological relations
depends on the sargasso. Toxic dinophytes frequently grow on the it,
making its consumption dangerous. Some animals in this unusual community
adopt an appearance similar to the alga, and this mimicry of the
sargasso may thus provide them with some protection. The density of
Sargassum in the regions where it accumulates does not usually exceed
0.6 to 1.6 g per square meter.

Another type of community, comparable to phytoplankton, consists of
the organisms in the polar ice in the saline liquid between the grains
of ice making up the polar pack ice, which, as a mass, behaves like a
plastic material. They are microscopic algae that are partly the same as
those of plankton, partly algae of the same groups, but whose behavior
is more benthic (Amphiprora, Frustilia, etc.) and are similar to some
species that also live on the sand of beaches or littoral sediments.

Making sure of permanence

Just as in a river every population eventually multiplies locally
in a way that adjusts to the risk that its members run of being eaten or
carried away, so in exactly the same way in plankton the rate of
reproduction and the probability of sinking from the initial level
eventually reach some sort of balance. In passive phytoplankton, a
fraction of the population is continuously being lost, and it is
essential that conditions are present (light, nutrients) that allow
sufficient reproduction for populations to persist. However, those
species whose members can maintain themselves at a specific level, for
example by swimming, and have some defense against potential predators,
can thus "negotiate" within the eternal bargaining of natural
selection some reduction in the rate of reproduction required to
maintain their populations. A broader point of view would relate the
time needed for the renewal of the population or for the persistence of
ecosystems (from days to weeks in the phytoplankton, and years or
centuries in a forest) to the time that sets the framework within which
can be described the important changes or deformations that occur in
their physical medium (from minutes to years in the oceans, from decades
to million of years on the continents).

Planktonic populations, especially autotrophic ones, are highly
transitory. Furthermore, the sea's structure is very complex, at
all scales, from the global to the small discrepancies and vortices that
appear in measurements taken continuously from a vessel or buoy, whether
drifting or under power. Discontinuities are maintained between
different and/or confluent volumes or masses of water if there is a
renewal of either or both of the water masses in contact. Under these
conditions it is probable that interesting things, such as an increase
in production, will occur. A three-dimensional interpretation and
explanation of distributions should be sought that is compatible with
the lineal information obtained from exploratory transects. Nowadays,
this is complemented by remote detection from space. The distribution of
plankton is not random and its organization can be interpreted at all
scales of space and time.

The productive zone is a relatively thin surface layer, but a good
part of the phytoplankton sinks and is consumed at depth. Migratory
zooplankton is very effective at bringing about a relatively uniform and
constant redistribution of the few morsels of nourishment in the form of
plankton that reach the inhabitants of the great depths. The ocean is an
example of an ecological system whose activity is maintained by a
relatively sparse surface layer, and which is only about one hundredth
of the thickness of the water whose life it sustains. This means that
the return pathway of the chemical elements will be difficult, and total
recycling slow. This alone would be enough to understand why marine
primary production is, per unit area, only about a third of that on the
continental surfaces. Moreover, only about 5% of total marine primary
production can be attributed to the coastal benthos.

2. Primary producers: the phytoplankton *

2.1 Phytoplankton organisms

Phytoplankton consists of unicellular autotrophic organisms and
also includes others that are clearly derived directly from autotrophic
organisms, even if they are clearly totally or partially heterotrophic.
They are small (generally between 2 and 200 microns and occasionally
more then 1 micron) and in many species, the cells, although still
autonomous, form chains or filaments, sometimes covered in mucilage,
that may be visible to the naked eye.

Cyanobacteria and protochlorophytes

The smallest members of the photosynthetic plankton are the
cyanobacteria (formerly cyanophytes or "blue-green algae"),
prokaryotic organisms that are usually round (Synechocystis) or
elongated (Synechococcus), and approximately 1.5 microns in diameter, or
less. These organisms are slaves to the viscosity of the water, and can
only renew the few micrometers of water around them with great
difficulty. If they are actively sought, they are found almost
everywhere, in concentrations that may reach hundreds of thousands of
cells per milliliter, although densities are normally much lower.
Preliminary studies exaggerated their role in total primary production,
although they may account for between 20-40% of the total (often less),
depending on their greater or lesser local abundance. Their nature and
persistence means they are found almost everywhere, in a more or less
inactive state, in a great depth of water, ready to photosynthesize when
the water reaches sunlit levels. These organisms may be consumed,
together with other bacteria, by relatively abundant and diverse small
heterotrophic flagellates in the plankton.

The pigments of cyanobacteria are found on thylakoids at the edge
of the cell and not in discrete chromatophores, and this gives the cells
a diffuse color. They contain chlorophyll a and several phycobilins and
carotenoids. These phycobilins confer on them the distinction of being
the only members of the phytoplankton that can photosynthesize using the
radiation in the intermediate band of greenish light. In addition to the
cyanobacteria, there are other prokaryotic organisms in the
photosynthetic plankton that, given their small size, (between 0.6 and
0.8 microns) look similar but possess chlorophyll b. They are
protochlorophytes, also found throughout the oceans. Their organization
has been compared to that of a plastid surrounded by a cell wall.

In freshwater, cyanobacteria with larger cell sizes--and thus an
organization even further removed from that of other prokaryotes--are
common and diverse, although this is not the case in the sea, except for
some of the less saline areas of the Baltic Sea. One of the few
exceptions is the genus Trichodesmium, which forms long filaments joined
together in bundles and is especially frequent in stratified tropical
waters, usually outside or on the edge of upwellings. It has been
stated, although not universally accepted, that this organism, like most
other cyanobacteria, can fix atmospheric nitrogen. Obviously, the
insignificant presence of these cyanobacteria in the open seas must be
considered evidence that nitrogen is not a major limiting factor in the
open ocean. On the contrary, these cyanobacteria thrive in fresh water
undergoing denitrification and rich in phosphates, situations brought
about nowadays mainly by human activity.

The filaments of Trichodesmium are visible to the naked eye, and
support other organisms, such as hydrozoans and even fungi, which
potentially make them a kind of pelagic lichen. The masses break up
quickly when the water is agitated, and when the filaments separate they
are no longer visible. Richellia forms short filaments, generally with a
heterocyst (a differentiated nitrogen-fixing cell) at one end, and they
are usually found as internal symbionts within larger diatom cells.

Dinophyta

Dinophytes (or Pyrrophyta, Dinophyceae, Dino-flagellata or
Dinomastigota) ** are eukaryotic, but with an unusual, especially
primitive nucleus whose chromosomes lack histones and are permanently
condensed. These chromosomes are usually clearly visible during the
interphase of division and make the nucleus look like a ball of string,
possibly a useful character when identifying unknown cells. Different
species show differing levels of polyploidy and may show polymorphism in
size, with an apparent increase in the frequency of larger cells during
the cold season.

The organization of the dinophytes is extremely varied; they form a
group with a remarkable evolutionary capacity, and are probably the
oldest of the forms that now dominate the plankton. However, they have
not developed true multicellularity. They could be considered as a
potential phyletic lineage that aborted, probably because other forms of
organization (i.e., the true eukaryotes) arrived first. The few forms
that have attained some form of multicellularity are parasites of
planktonic animals, such as copepods and tunicates.

The dinophytes as a whole now show a very wide functional range
that is more diverse in the seas than in freshwater. They range from
autonomous photosynthetic organisms that normally possess flagella, to
large cells 0.5 microns that behave essentially like animals. The genus
Noctiluca even ingests "higher" animals, such as tunicates or
the eggs of anchovies. The most primitive--and most common--dinophytes
possess chromatophores with chlorophyll a and c and carotenoids
(peridinin and other specialized compounds). They are generally
yellowish green or brownish green in color, but the blooms of some
species appear reddish ("red tides").

The cells of dinophytes are always asymmetric. The commonest shape
in the most numerous families consists of an equatorial girdle twisted
at the ends (forming a right- or left-handed helicoid) that meets or
intersects with another longitudinal girdle (the sulcus or groove). The
bases of two more or less differentiated flagella are located where the
two grooves meet. Pseudopods of clear cytoplasm may form in this special
region and are either linear or take the form of a large feeding
membrane for extracellular digestion. This region is also where the
intracellular cavities (pusules) open. Other advanced features are found
in some dinoflagellates, such as ocelli, which are able to perceive
light, and tentacles of varying maneuverability. Many species are
capable of emitting light, often through specialized organelles
(scintillons).

Very potent specific toxins that vary greatly in their chemical
composition and produce ill effects on some animals, are produced by
many dinophytes, including the planktonic genera Prorocentrum,
Dinophysis, Gonyaulax, Alexandrium, Pyrodinium, as well as Gambierdiscus
and some forms of Prorocentrum that live on Sargassum, on other
macroscopic marine algae and even on grains of sand. These varied
compounds (such as saxitoxin) are molecules with rings containing
nitrogen, and a molecular weight that is normally greater than 1,000
daltons. These substances may reach human beings (see p. 239) via the
organisms that eat them, usually lamellibranchs (food poisoning as a
result of eating mussels or clams) or fish ("cigatuera fish
poisoning" in some tropical countries). Some, such as Cochlodinium,
form rod-shaped bodies (trichocysts) of different sizes that can be
rapidly extruded and form sticky filaments (possibly also poisonous)
that stick to and harm the gills of fish.

The surfaces of dinophyte cells have variably shaped covers,
ranging from simple membranes, to complex structures consisting of
several different plates joined by complex sutures. Sometimes the cover
includes a pre-formed region through which the cell, after adopting a
spheroid shape and enclosed within a new relatively thin covering, can
abandon the old cover, like a pilot ejecting from a fighter plane. The
cell may enter a quiescent state during which its covering becomes
thicker and accumulates materials similar, at least in terms of their
resistance, to the sporopollenin of the walls of pollen grains and other
plant spores. This allows it to be preserved for long periods. In other
dinophytes the outside is calcified.

A good fossil record exists for the dinophytes, proof of the
group's antiquity; the remains of dinophytes similar to
contemporary species are known from the Silurian and similar forms, such
as some acritarchs, are even older, dating from the Cambrian period or
before (see volume 1, p. 105). Their age is also shown by the fact that
the corals (and other marine animals) adopted them as symbionts long
ago, at the evolutionary origins of symbiosis. These surprisingly
uniform symbionts are generally identified as Symbiodinium
pseudoadriaticum. The careful study of symbionts from different hosts
shows that the differences between strains are minimal.

Dinophytes or dinoflagellates are found everywhere in contemporary
marine plankton and are represented by organisms generally 10-200
microns in size that vary greatly in their forms of feeding. There are
more heterotrophic forms than might be thought, with internal feeding
(ingestion) and external feeding (the feeding membrane found in many
Protoperidinium). They may contain internal or semi-external symbionts
(such as the cyanobacterium Histioneis). The advanced assimilation of
some symbionts through dinophytes has led to the evolution of chimaeras
or mosaic organisms. Dinophytes with heterotrophic nutrition are
especially diverse and abundant in the so-called "twilight
zone," below the chlorophyll maximum in stratified waters.

The transverse flagellum makes the cell rotate around its
anterior-posterior axis. The prefix "dino-" in dinophyte is
derived from the Greek root dinos meaning to spin like a top, and not
from deinos, meaning terrible, as in dinosaur. The transverse flagellum
is normally more robust and often acts against the irregular or
flattened shape of the cell. This usually bears a wealth of detail
(Ceratium, Dinophysis, Ornithocercus, etc.) although all show an unusual
asymmetry. The flagellum's opposing action increases water flow
over the cell, leading to increased absorbtion. At the same time, the
movement of the longitudinal flagellum allows the organism to maintain
itself at appropriate levels of light and nutrient concentration within
the water, and even to undertake moderate vertical migrations.

Cryptophytes

The cryptophytes ***, in a sequence of increasing cell complexity
and size, are generally small, normally between 5 and 20 microns, and
more or less elongated, asymmetric cells, often pointed at the anterior.
Their two flagella emerge from a type of "gullet" and are
associated with ejectosomes, "rods" that fire like the
trichocysts of dinophytes. They also possess chromatophores with complex
pigments, and thus vary in color: greenish, reddish, or even bluish and
pinkish forms are found. There are heterotrophic forms, some of unknown
descent, such as the very common colorless organism Leucocryptos marina,
and others that eat bacteria. It has been shown that many cryptophytes,
and maybe all, are really chimeras, or compound organisms, whose former
symbionts have been assimilated into the organism.

These organisms used not to be mentioned much in discussions of
marine plankton, but they are, in fact, frequent. They are often found
forming discontinuous swarms in surface water, often after intense local
mixing. The most important genera are Cryptomonas, Rhodomonas and
Hemiselmis.

Chrysophyta or chromophytes

Rather than referring to a specific taxonomic group, this catch-all
collective name is used here to include, in addition to some less
important groups, the groups of haptophytes (including
coccolithophorids, diatoms, and silicoflagellates) that will have to be
reclassified when they are better known and a consensus has been reached
on the affinities of these diverse flagellates, now more widely studied
thanks to electron micros-copy ****. In general these organisms have
yellowish chromatophores (chlorophyll a and c and fucoxanthin are the
basic pigments) that never accumulate starch as a reserve, with
differentiated flagella (when present), clear plasma, and a cell
covering of small scales rich in structural detail, some of them
mineralized, that may extend to varying degrees over the flagella. Their
study requires the use of electron microscopy, and for technical reasons
reliable information on their distribution is necessarily relatively
recent. The diatoms (Bacillariophyta) are included in this group and are
relatively large and possess silica covers. As has been known for more
than two centuries, this covering, or frustule, consists of two halves
(the valves), one of which overlaps the other like the lid on a box. The
large size of the cells, the nature of the valves, the absence of
flagellate forms (except in some heterogametic forms) and the diploid
nature of the vegetative cells has meant that the diatoms have been
considered the zygotes of other chrysophytes. They are also relatively
more recent; their greatest expansion took place at the beginning of the
Tertiary period, and might be related to the development of marine
regions with intense upwelling. The diatoms are, in short,
post-dinosaur.

The haptophytes or prymnesiophytes

The haptophytes or prymnesiophytes are a group of chrysophytes,
quite small in size (10-25 microns) that normally possess two functional
flagella, and a third filament (the haptonema) that is often coiled into
a spiral. The haptonema's function and structure are unlike that of
a flagellum, as they lack the two central and nine peripheral pairs of
tubules found in normal flagella (see volume 1, p. 90). The name
haptonema suggests they might serve to fix the cell to a substrate, but
in some prymnesiophytes (Chrysochromulina) they serve to attract and
guide the bacteria they eat, thus making ingestion easier.

Phaeocystis cells may bear flagella, although the most common form
consists of very small (2-4 microns) spherical cells immersed in a
mucilaginous matrix that may form important masses and block the mesh in
plankton nets and even the gills of fish. North Sea fishermen have long
known that fish flee from areas where Phaeocystis is abundant. It is
regularly found in the Mediterranean, but more frequent or larger blooms
occur in colder seas, even in the seas around the Antarctic, where their
abundance was thought to be due to the scarcity of bacteria in the
digestive systems of the animals that eat material synthesized by them.
Phaeocystis and some species of Chrysochromulina are toxic and there was
considerable alarm in summer 1988 (and the following years) when a
species of Chrysochromulina reached local concentrations of 80,000 cells
per micron in the North Sea. The many species in this genus range from
the simplest, a few micrometers long, to ones 13 microns or more in
diameter.

The most important group of autotrophic and planktonic haptophytes,
important primary producers, is without doubt the coccolithophorids,
whose cells are covered with scales of calcium carbonate called
coccoliths. Most of these cells do not possess functional flagella.
There are cases of polymorphism, in other words, alternation between
different forms of organization, or at least between forms bearing
different scales. The coccolithophorids with the most highly devolved
scales (Scyphosphaera, with calcareous scales that look like cut-glass,
Rhabdosphaera, Discosphaera, etc.) seem to appear towards the end of
ecological successions, when cells divide more slowly and prepare to
deposit calcium carbonate, and possibly other related chemical elements.
Species that multiply extremely quickly (such as Emiliana huxleyi,
without a doubt the most common organism in the marine plankton, and
possibly the entire world), have thinner scales (the greater the rate of
cell division, the thinner and more easily segregated the scales), and
are usually only a few micrometers in size. Consequently, they are
difficult to study and identify using a normal optical microscope. More
than 80% of the coccoliths that accumulate in the sediments of the
Mediterranean are E. huxleyi. Coccolithophorids multiply quickly in
appropriate conditions, often close to fronts. It has been said that
some water turbulence observed from planes, for example in tidal fronts
to the west of the English Channel, is due to the proliferation of
coccolithophorids. The presence of calcium carbonate plaques may
increase cell density and help them to sink in rising water. They
contain carbon that is removed from circulation when the scales or
coccoliths sink, thus reducing the greenhouse effect to some extent.
Coccolithophorid species are very ancient and widespread, and have
changed regularly over geological time, making their fossils suitable
for studying the distribution and diversification of plankton types over
long periods of time.

Bacillariophyta or diatoms

The other important group of chrysophytes is the Bacillariophyta,
or diatoms. Since their discovery, these organisms have attracted
attention because of their siliceous covering, often preserved in
ancient sediments. The surprisingly detailed and delicate structure of
the frustules could be seen with the optical instrumentation commonly
available in the 19th century. Studying diatoms became a hobby, the
first step of which was to boil the diatoms in acid to clean the
frustules. Thus a lot of work has been done on the taxonomy of the
group, now possibly over-detailed and with an excessive number of
synonyms. The same situation has happened with other organisms, such as
the mollusks, which have the good or bad fortune to bear hard parts.
Electron microscopy has helped to identify many of the small structures
of the frustule, some of which may be of great importance in
understanding specific details of the diatom's life. The frustule
is not inert, and its complex of pores and chambers may play a
significant role in nutrition. It often channels the production of
filaments of mucilage that join the cells together or swell to form
large mucilaginous masses (Chaetoceros socialis, Thalassiosira). The
organic matrix of the frustule deposits hydrated silica (SiO2 x nH2O),
or opal, polymerized in the form of a continuous molecular network.
Organic material occupies the free valencies, at least in the form of an
external film, and prevents the frustules from dissolving in alkaline
water that is not saturated in silicon. The siliceous part varies in
thickness depending on the species and on the conditions in which it
lives; each population shows variation in thickness and silicon is
rarely a serious limiting factor. The cells are often only slightly
silicified and apparently flexible in marine plankton, especially if the
diatoms are growing rapidly or if the silicon content of the water is
low (as in the Mediterranean, where alkalinity is slightly higher than
the ocean average, and where calcium concentration is also higher). In
the Mediterranean, only the thickest frustules are preserved in the
sediment, often proceeding from the littoral, as is the case in the
widespread Paralia sulcata or the resistant forms (hypnocysts) of
Chaetoceros and some other common genera. The valves of freshwater
diatoms also frequently reach the sea.

Diatoms are generally large organisms, reaching a size measured in
millimeters. They are divided into two main groups: centric and pennate.
Centric forms have valves showing radial symmetry, and oogamous
reproduction. The pennate forms have elongated valves and their
reproduction does not involve forms bearing flagella, but usually shows
formation of gametangia that copulate as a whole. There is also
Phaeodactylum, a curious organism with just one valve, that is common in
pools on rocky shores and thrives in aquaria, but which is only found by
accident in the open sea. Most marine planktonic diatoms are centric,
mainly belonging to the genera Thalassiosira, Coscinodiscus,
Chae-toceros, or Rhizosolenia (now subdivided). The pennates are usually
coastal, such as Asterionella, Thalassionema, and Thalassiothrix.

Diatoms used to be considered the marine equivalent of grasses,
innocuous and generous producers, with the sole vice of depositing
silica. Recently it has been learned that some species of Nitzschia
produce potent toxins, such as domoic acid, an amino acid that among
other effects may lead to amnesic shellfish poisoning in humans. The
cells of some larger diatoms, mainly of the genus Rhizosolenia, which
are vacuolate and float in nutrient-poor waters during the summer, house
nitrogen-fixing cyanobacteria (Richellia intracellularis). Other diatoms
are associated with ciliates that help to maintain them in suspension.
Chains of empty cells of diatoms of the genus Dactyliosolen are often
found bearing flagellated cells; these have been given the name of
Solenicola, but it is suspected that they could belong to the same
diatom's life cycle.

Dictyochophyceae or silicoflagellates

The silicoflagellates are medium-sized flagellated protoctists
(20-70 microns), with a thin membrane, numerous chromatophores and a
highly distinctive internal reticulate skeleton, generally showing
four-fold or six-fold symmetry. They are made of tubular structures of
silica (opal), which is more compact and is preserved better than the
frustules of diatoms. A second skeleton that forms within the cell
before division is the mirror image of the existing one, except in some
populations that lose their skeleton in periods of rapid growth. Fossil
remains have been found dating from the end of the Mesozoic period and
their expansion has been parallel to that of the diatoms, although
silicoflagellates are very morphologically conservative and
species-poor. Among the most common forms, the quadrangular Dictyocha
fibula is always slightly more thermophilic than Distephanus
(=Dictyocha) speculum.

The prasinophytes

The true green algae (Chlorophyceae) are freshwater organisms that
contain starch, and are colored green by the chlorophylls they contain.
In the marine plankton, we find the prasinophytes, a sister group,
ecologically parallel to the chlorophytes but distinguished from them by
cytological characters *****. There are many species with four equal
flagella (Pyramimonas, Tetraselmis) and covered with superficial scales,
even on the flagella. Species of the genus Halosphaera have quite large
spherical cells (40-100 microns in diameter) that form multiflagellated
propagatory cells.

The euglenoids and raphidophytes

The euglenophytes ****** are flagellates with a complex structure,
whose cover is made of interlocking elastic strips that allow continuous
deformation of the cell. They generally have two flagella, or at least
one that is functional if the other has been secondarily reduced. They
have green pigments and a glycide reserve (paramylon). They are common
in the marine plankton of eutrophic waters, such as ports. Eutreptiella
gymnastica is a typical species.

Another phylum of protoctists living in conditions similar to the
euglenophytes is the small group of raphidophytes *******, represented
mainly by the genus Chattonella, which probably includes some species
first described by the generic names of Olisthodis-cus and Hornellia.

Symbionts with simplified organization

Complete cells that can be considered as members of one of the
groups already described (such as cryptophytes) and other cells showing
varying degrees of simplification (often reduced to simple
chromatophores) are found as symbionts in ciliates (Mesodinium) and in
other organisms.

Cells that have not been simplified or modified, whose affinities
can still be recognized, live within foraminifera, acantharians, and
radiolarians. They may make a large contribution to primary planktonic
production and many of their host organisms have attained a level of
trophic independence comparable to that of corals. Several of the
organisms in the dinophytes and cryptophytes are really chimeras,
consisting of associated components of very different genetic origin.

2.2 Phytoplankton distribution and diversity

The density of phytoplankton populations (microplankton and
nanoplankton) in the photic zone is usually between 10 and 1,000 cells
per milliliter. Many are cells of partially or totally heterotrophic
organisms. The number of picoplankton cells (cyanobacteria and
protochlorophytes) may be 10-1,000 times greater (104-106 per
milliliter) but they are extremely small organisms, each of which is
only about one thousandth of the average volume of nanoplankton.
Populations in deep waters are sparser, although it is impossible to say
how far down they are found. Cells of various species are always found
at depth, out of reach of light.

The small cells of the picoplankton or ultraplankton rarely receive
specific names and at most a generic name, although it is known that
there are different forms since not all populations behave the same in
culture. The larger organisms are easier to describe, and their study
began and progressed at a time when taxonomy was considered more
important than now. The classic works and very detailed monographs
published between the end of the last century and the middle of this
century have beautiful illustrations. Many species have never been
described, which becomes obvious to anyone investigating phytoplankton
in detail in any specific location. Many groups, such as the
cryptophytes and several groups of small flagellates (including some
with hard parts, such as coccolithophorids) are particularly not well
known, and the same is true for the numerous and frequent heterotrophic
dinophytes found in the penumbra levels.

Low diversity, wide distribution

Alain Sournia and collaborators published in 1991 a census of known
species of marine phytoplankton and gave a very low figure of less than
5,000 species, far less than the number of known freshwater plankton
species. This relative poverty is surprising, especially when compared
to the large number of species found in any family of insects. This lack
of species in the oceans may be due to the intense mixing of the water,
which has the effect of countering genetic isolation. Lakes may well
have been more effective at confining populations and promoting
speciation. Even so, the marine planktonic "flora" has changed
quite quickly over geological time and is not charcaterized by a low
level of speciation.

In conclusion, biological diversity may be lower than expected,
even though not all species are found everywhere. Without doubt, the
continuity and movement of the oceanic waters help to reduce the
separation and speciation that reflect past history and geography in
continental or freshwater environments. It is clear that our knowledge
is still limited because of the lack of accurate descriptions and only
limited use is made of taxonomic criteria based on genetic and
biochemical differences. It cannot be denied that there are many species
of southern diatoms and that many dinophytes, mainly of the genera
Ornithocercus, Amphisolenia, and Histoneis, have only been found in the
highly stratified waters of tropical seas. Some of these organisms, such
as Dinophysis miles, even show "clines," or gradients, in
their shape over large areas.

Planktonic ecosystems

Certainly, planktonic ecosystems are not as diverse and clearly
established as tropical rainforests or the arctic tundra, but each area
of ocean does have its own set of conditions and its own dynamics, and
this defines the relative abundance of different species.

There appears to be no problem maintaining a "genetic
bank" rich enough to allow effective colonization of water in any
new situation that may arise. There has been speculation about the
possible importance to blooming of the availability of enough resistant
cells in the bottom sediment of blooming areas. Although present, these
cells may not be indispensable, because detailed studies of widely
varying places always show live cells of most, if not all, the usual
species of the local flora that proliferate alternately during the
course of annual or seasonal successions. Quiescent cells are relatively
numerous in deep waters, where they are still alive even though they are
obviously not photosynthesizing.

If the number of species is relatively restricted and geographical
differences are small, then clearly similar communities may be found in
very different locations. If we are able, or wish, to distinguish
between different communities, then they often represent different
stages of the ecological succession typical in plankton, starting from
populations showing low diversity and often rich in diatoms (or
coccolithophorids), to situations where populations are locally
heterogeneous and show higher diversity, especially of dinophytes.

Taxonomy is not fashionable and studying phytoplankton organisms is
often very difficult because they are small and fragile and their
fixing, sectioning, and study using electron microscopy requires, at the
very least, patience, skill, and time. Other aspects of modern biology
such as studying the possible existence of clones or different races
within each of the "classic" species, mainly shown by
biochemical and physiological differences, have a more positive impact
on the analysis of phytoplankton populations. The "species"
where these races or clones have been sought are those of genera such as
Phaeodactylum, Emiliana, Gonyaulax, Skeletonema, Thalassiosira, and
Prorocentrum, which are most commonly cultivated in laboratories. They
show physiological differences between strains with respect to
temperature and salinity, heterotrophic capacity, vitamin requirements,
and other properties that clearly define their relative probabilities of
survival in a marine environment that is never uniform.

There are some well-known differences between comparable pairs of
species, such as Ceratium furca and C. fusus, that occur together but
which diverge in terms of their preferences. C. furca is more
thermophilous, less halophilous, requires more phosphorus, and
multiplies more actively at the surface. A further example is the
differences between Nitzschia delicatissima and the species of the
seriata group of the same genus, which are found in colder, deeper
waters, with higher salinity and phosphorus levels. Local observations
repeated over time suggest many other similar ecological divergences. In
pairs of organisms with very simple morphology, such Synechocystis and
Synechococcus in the phytoplankton, biochemical, physiological and
genetic techniques are required to illustrate these differences.

Census information from a single region can be plotted on a graph
showing the logarithms in decreasing order of the number of individuals
of a species, arranged from more to less frequent, thus giving a good
expression of diversity. This method sometimes gives surprising results.
For example, the Mediterranean turns out to have one of the greatest
diversities, greater than any comparable sea, and even greater than more
"tropical" ones, such as the southern part of the Caribbean
Sea. This difference is consistent with the fact that the density of
plankton and its productivity is slightly higher in the Caribbean than
in the Mediterranean.

Diversity and production

In general, there is an inverse relation between diversity and
biological production and even more so between diversity and
fluctuations in production, whose frequency and intensity in the oceans
shows a strong correlation with production. The periods of peak
production are typically characterized by populations with one or a few
very abundant (in reality dominant) species, and there is a long list of
species in reserve, represented by only a few individuals.

These relationships can be visualized by graphically representing
the relations between the number of individuals and the number of
species. These show the irreversibility nature of all real changes,
especially those dealing with living systems. Increases in biomass--and
total plankton density--are due to just a few species. Once maximum
biomass has been attained, the number of contributing species increases
and, eventually, the biomass present decreases but sufficient numbers of
individuals of certain species are still spread about to serve as a
basis for future growth and spread.

This mixed, species-rich population, although mostly quiescent,
might be compared to a "seed bank," and is located in dimly
lit water, and so it is at this level that maximum overall diversity is
often found, which is the asymptotic ceiling of the spectra of various
localities. This is comparable to persistence mechanisms in rivers,
where a sizeable reserve of propagules of many different species is
available on the sides of rivers and at different water levels, often in
very thin soil or even far from the flowing water, and this is the
explanation for the continuous recolonization of mountain streams and
seasonal rivers.

This highly diverse reserve is made up, in an alternating and
discontinuous fashion, from the results of the evolutionary experiments
continuously undertaken in the more active parts of the ecosystem. These
ecological, genetic, and evolutionary experiments will, if relevant,
enrich the genetic diversity of the reserve over time. This is one of
the functions of the rapid and abundant phytoplankton blooms that are
always taking place somewhere in the ocean.

2.3 The primary production of phytoplankton

The primary producers of plankton are small. Most measure between 2
and 200 microns, and because they do not have fibers, nor vessels, or
wood, they allow us to understand the question of production better than
does terrestrial vegetation. They are suspended in water, where they
obtain food and nutrients.

The photosynthetic pigments

Chlorophyll and other pigments active in photosynthesis are easily
extracted with the appropriate solvents, and easily measured by
colorimetry or fluorescence. In volume 1, pp. 180-190, information is
given about the distribution of light within the water and about the
structure and function of the photosynthetic apparatus that is
applicable to the biology of the phytoplankton. In marine phytoplankton,
the ratio of the total weight of chlorophyll (which contains 44% carbon)
and total weight of organic carbon is generally between 1:30 and 1:300,
a much higher proportion than that found in terrestrial vegetation, as
the latter contains a high proportion of support and transport
structures that are disproportionately rich in carbon.

The American biologist Alfred C. Redfield proposed for
phytoplankton an average ratio between the relative concentrations, in
atoms, of C:N:P (carbon, nitrogen, and phosphorus) of 106:16:1, which is
generally accepted and widely used. Multiplying by the respective atomic
weights gives the ratios by weight. In terrestrial vegetation, the
relative quantity of carbon is at least two to five times greater, a
ratio that agrees with the statement in the previous paragraph. It is
thus not correct to compare the phytoplankton to the grass in a field
that has been ground up and in suspension. For the comparison to be
correct, the ground-up material would have to be limited to the
photosynthetic tissues of the leaves. Terrestrial vegetation usually
contains 1-1.5 g of chlorophyll per square meter. In the oceans, the
active phytoplankton is in a layer about 100 m thick, approximately the
same as the height of the tallest trees, but the quantity of chlorophyll
present is smaller and normally does not exceed 0.1 g per square meter.

The pigments present in the photosynthetic systems mean that the
effective photons are those between 400 nm (blue) and 800 nm (red): This
is the active radiation in photosynthesis. There is a relative gap in
the absorption by the pigment at the wavelength at which water is most
transparent (greenish blue), centered around 520 nm. Only phycobilins
found in some cyanobacteria can absorb radiation in this segment of the
solar spectrum. It is surprising that this window is so little used, as
cyanobacteria are relatively infrequent in sea waters, unlike in the
waters of the continental surfaces, where they are very abundant. This
radiation is correctly expressed as energy or is counted in photons
(mE), which is justifiable because it seems that all photosynthetically
active photons are about as effective, independent of their respective
energy. The vertical distribution of available light is a function of
the water's transparency. There is a critical zone between two and
two-and-a-half times the maximum depth at which a Secchi disc can be
seen, and coinciding with the chlorophyll maximum, where a considerable
part of production takes place. The carbon assimilated per gram of
chlorophyll rarely exceeds 4 g per hour of light, and decreases rapidly
(logarithmically) below 60 (mE per square meter per second (about 8,000
"lux").

Production is studied using oxygen exchange, or radioactively
labelled carbon (14C) in small confined volumes of water with its
plankton. Photosynthesis includes a reaction that is photochemical and
is thus less dependent on temperature than the later metabolic steps.
The speed at which the nutrients contained in the seawater are consumed
makes it possible to fill in the picture. On the basis of pigment
concentration, or more accurately fluorescence, attempts have been made
to estimate production. The search for an indicator of real production
that could be perceived from space is understandable, but at the moment
the relationship between potential productivity and real production is
indirect and unreliable.

The role of nutrients

If we draw up two parallel lists to compare the concentrations of
the different chemical elements in organisms and in seawater and their
respective quotients, phosphorus is nearly almost always the relatively
scarcest element, and thus the one that limits or controls production.
As in an industrial production line, the speed of the operation depends
on the component present in the least proportion. Carbon never appears
to be limiting, unless, as occasionally occurs in certain organisms, it
is for some specific physiological reason. The elements that make water
saline--such as calcium, magnesium, strontium, sodium, potassium, and
fluorine--are never limiting. It is not clear how and why many marine
planktologists have, for some time, appeared to consider that the
element that most frequently limits primary marine production is
nitrogen (Harvey, in 1955, correctly considered phosphorus more limiting
factor than nitrogen). It is true that the quantity of dissolved
combined nitrogen (nitrate, nitrite, ammonia) may be relatively small,
often as a consequence of bacterial denitrification that converts the
nitrogen from a combined state to its molecular state which, because it
is a gas, dissolves in water. This gas molecule (N2) is in equilibrium
with the atmosphere, and so seawater normally contains about 13 mg
(=10.5 [cm.sup.3]) of nitrogen per liter. The level of combined forms of
nitrogen dissolved in seawater is usually only 1/100 to 1/1,000 of the
concentration of gaseous nitrogen. If nitrogen was the limiting factor,
it is difficult to believe that there would not have been a more massive
invasion of the phytoplankton by cyanobacteria, as has happened in
continental waters and is now evident in waters enriched in phosphorus.
There is not enough combined nitrogen in these waters and cyanobacteria
fix atmospheric nitrogen, so that eutrophic lakes are filled with them.
Cyanobacteria are present in considerable numbers just about everywhere,
although in the sea significant visible blooms of filiform cyanophytes
(Trichodesmium or Oscillatoria, Nodularia) are scarce, and they are
often found precisely where combined nitrogen is not lacking, perhaps
due to the previous activity of these cyanobacteria populations.

Phosphorus concentrations are low and are decisive for water
fertility. Although the unlit levels of the oceans contain a
considerable reserve, with concentrations of 30-60 mg per cubic meter
(in the Mediterranean as low as 5 mg per cubic meter), in the
illuminated strata the action of organisms often maintains the
concentration of phosphorus at undetectable levels. Part of the
phosphorus available to organisms is in relatively unreactive organic
forms, making it even more difficult to measure. Phosphorus
concentrations in surface water are usually negligible; when more
arrives, it is rapidly used up.

The behavior of nitrogen and phosphorus show marked contrasts (see
volume 1, pp. 129 and 165-166). Nitrogen forms soluble compounds and
circulates between the water and the atmosphere. Phosphorus, on the
other hand, is found in organisms in the form of compounds of phosphoric
acid, never reduced to the element, and in seawater it is found combined
with organic bases or as orthophosphate (HPO4=). As its compounds are
relatively insoluble, it cycles basically between the water and the
sediment, where it is continually being lost or immobilized. In the
dynamic of the biosphere, phosphorus acts as a major regulator, or
"buffer."

All sediments contain phosphorus, especially those formed under
very productive water (in upwellings), and these sediments are rich in
phosphorites. In these regions, seabirds obtain phosphorus from the
oceans and temporarily immobilize it in guano, thus reducing the
productivity of the pelagic systems they depend on. This behavior is
equivalent to that of the small migratory planktonic crustaceans whose
compacted excrement also slows down global dynamics by accelerating the
export of phosphorus to the depths. It is as if the phosphorus cycle
always has to pay some price.

This type of regularity is not always welcome. When attempts have
been made to artificially fertilize marine areas, it has been found that
a considerable part of the phosphorus is lost in the first cycle,
precipitating as insoluble phosphate, and so it is not possible to
stabilize production at desirably higher levels. The continuity of life
requires the redissolution and mobilization of more phosphate, and this
occurs, to a large extent, on the continents.

Significant correlations are not established between
concentrations. Instead, they should be based on suitable processes, for
example, the consumption of phosphate and plankton growth. This
relationship is naturally that of an asymptotic process, slowing down as
the mass of organisms increases and the concentration of the element
being assimilated diminishes. Moreover, there may be further limitations
at any given moment, but this does not exclude the possibility that
other elements or compounds are present in excess.

A widely used indicator is the concentration of an element that
shows an absorption velocity that is half the maximum possible value. A
typical phytoplankton cell contains between 0.3 and 2 pg (picogrammes, 1
pg=10-12 g) of phosphorus, and the concentration of semi-saturation may
be between 0.02 and 0.5 mg at P per liter or mM P (i.e. between 0.6 and
15 mg of phosphorus per liter). Nitrogen has a semi-saturation constant
that varies depending on the type of ion or molecule assimilated, but is
about ten times greater than that of phosphorus, which is not surprising
if we remember the relationship advanced by Redfield.

It has often been considered that the chain of production could be
broken by the scarcity of some essential element other than phosphorus
or nitrogen. This might be a micronutrient such as cobalt, selenium, or
the others that appear to be necessary for marine plants and animals.
Seawater is a sort of extract of the Earth's crust and it appears
to contain all the elements in sufficient quantities, although there may
be relative shortages locally. In the 1980s iron was suggested as a
possible factor limiting phytoplankton growth, and it was suggested that
the southern oceans should be enriched with soluble iron compounds to
increase phytoplankton production. This would help to fix more carbon
and perhaps reduce the greenhouse effect. There are, however, no
convincing reasons for affirming that iron is a limiting factor
anywhere.

Marine phytoplankton also shows vitamin requirements and many
organisms require the presence in the environment of specific organic
molecules, already synthesized, such as cobalamines. However, this can
only rarely change the most common conditions of production because
there is always enough diversity of organisms available as a whole for
them to be able to produce in most given circumstances.

New production and recycled production

Primary production by the phytoplankton is the basis of life in the
seas. The oceans also receive a relatively small subsidy from the
continents in the form of the dissolved materials transported by rivers.
This is from 1-2 g organic carbon per square meter per year. Much of
this material cannot be directly biologically used and just slowly
decomposes in the water.

It is not easy to draw up a critical summary of the available
information about production. It has been suggested (see volume 1, p.
191) that the world average of carbon fixed per year per square meter of
section is about 100 g. This type of figure requires the correct
integration of a range of figures for production obtained at varying
depths from the surface to the lower limit of photosynthesis. Most
published data on oceanic production refers to net phytoplankton
production after deducting respiration by the algae, and in reality
these values show great uncertainty.

Experiments carried out to measure primary production highlight how
complicated it is by recycling and by the difficulties of quantifying
this. To carry out this type of measurement, the plankton and water are
usually confined within a flask. It is recommendable to remove the large
animals by straining the water through a mesh that allows phytoplankton
to pass, but retains the animals. All in all, this task is contradictory
or downright impossible, because there are algae, such as diatoms with
large appendages that are bulkier than many animals. Sometimes these
precautions are not taken and what is being examined in the confined
space of the flask is the metabolism of an entire system, whose
components cannot be distinguished. If we remove the large animals, we
are left with the small ones, and in any case it is impossible to remove
the bacteria, which cannot be separated in a physiologically practical
and effective way from planktonic algae. All experiments to measure
production, whether by oxygen exchange or by the use of 14C (perhaps
even harder to interpret), express the overall result of complex
biological activity, in which internal recycling of part of the elements
has never ceased. This difficulty is extremely obvious in highly
integrated symbiotic systems such as corals or some non-photosynthetic
planktonic protoctists that show negligible net production to external
observation, given that they recycle their chemical elements internally,
using energy provided by light.

It has been pointed out that the cycles in the Amazon show a
similar internalization, and thus provide almost no oxygen and absorb
almost no CO2. After all, the Earth as a whole recycles and we reach the
conclusion that the distinction between "gross" production and
"net" production is a consequence of the intellectual limits
we place on the entity in question and how we interpret it. The real
functioning of ecosystems makes many of our conceptual schemes
unworkable.

More pragmatically, pelagic space can be divided into overlying
strata. The level just below the limit at which light is sufficient for
photosynthesis is especially important because it separates an upper
photic region from a lower aphotic layer, the latter with very little or
no light. The normal functioning of the pelagic ecosystem results in the
net transport of nutrients downwards and their accumulation in the lower
compartment.

For the last few decades, it has been usual to expose collecting
devices, for one or two weeks at standardized depths, in order to gather
the material that is continuously settling, such as dead plankton or its
hard parts, excrement, material that arrives transported by the air
(pine pollen is found almost everywhere, for example), and so on. The
results are often unreliable due to the inclination of the recipients
and interference by horizontal currents, but it is generally found that
both the quantity of material and its nutritional value diminish with
increasing depth.

A considerable fraction of the elements (nitrogen, phosphorus,
etc.) are assimilated in the photic zone: The phytoplankton is eaten by
little animals, and these may excrete voluntarily or involuntarily (when
they are eaten) at the same or a lower level. Small primary producers,
such as cyanobacteria and other photosynthetic bacteria, are ingested by
tiny ciliates and flagellates in a cycle called "microbial"
because the organisms recycling part of the primary production are
small. These organisms may often be dispersed, but more often they are
associated with dead material in flakes, often large and visible as
"sea snow." The quantity of tripton (non-living, detritic,
organic material suspended in water) is about ten times that of
plankton. This goes unnoticed if we restrict our understanding of
plankton to what can be retained by the cloth of a sieve or net, and to
cyanobacteria and other tiny photosynthetic bacteria. This detritic
material in turn absorbs various organic compounds and can concentrate
the secretions of organisms. All in all, it is a different, but
important, twilight world.

To the previous elements we must add the part of primary production
that serves as food, mainly during the hours of darkness, for the many
small crustaceans that migrate alternatively from upwards and downwards,
leading to an even more definitive loss of essential nutrients from the
upper stratum. These crustaceans as such are less important than their
compacted excrement, which sinks quickly until it breaks up on reaching
considerable depths due to the action of the bacteria that are always
found adhering to the film that surrounds them and keeps them compact.
This of course only happens if the excrements are not captured for their
own use by needier copepods living at greater depths.

Below a certain depth, life only continues to exist because it
receives a contribution or subsidy from above (the only exceptions are
the "oases" at great depths, which are maintained by
chemosynthesis around submarine hydrothermal vents, described in chapter
3.5, section 1 of this volume). However, this manna would soon cease to
fall if the process of primary production was interrupted by a lack of
nutrients. The return of mineral nutrients to the surface is necessary
to avoid interrupting the production cycle and requires the energy
provided by oceanic circulation. This is called external, or exosomatic,
energy, to distinguish it from the internal energy or endosomatic energy
associated with light and the metabolism of organisms.

For every site and every season it is possible to measure, at least
in theory, a level corresponding to the "center of gravity"
around which the function of primary production is distributed, as well
as another barycenter, or center of gravity around which the respiratory
activity of the system is distributed. The difference between the two
mentioned centers of gravity is related to the average path taken by a
carbon atom from the site of assimilation to the site of respiration.
This distance is related to the degree of superimposition in the
distribution of the factors of production. These two centers of gravity
can never coincide, but they will be closer together in a highly
turbulent system, and will be further, possibly much further, apart in a
more stratified system. If we distinguish between compartments, all show
some internal recycling and an external circle made up of important
export routes that are equivalent if the situation remains more or less
stationary.

Naturally, the lower limit of the zone where photosynthesis is
possible is particularly appropriate for siting an imaginary or
conceptual frontier. There will always be some loss of organic material
downwards towards the unlit depths. If the situation is stationary for
more or less prolonged periods, this requires the entry into the
superficial compartments of equivalent supplementary nutrients (some P
and N), whether by horizontal transport, local upwelling, or seasonal
vertical mixing. This allows production considered as new, unlike the
production measured in the surface layers, which is associated with
biological recycling within the surface strata.

The ratio between new production and total production is usually
designated by the letter f, and this is an important local
characteristic of marine ecosystems. The value of f is high in
well-mixed systems and low (for example between 0.1-0.3) in ecosystems
that are stratified for long periods and that show relatively intense
upwards metabolic recycling, perhaps because selection has favored
organisms (swimmers) that have a lower tendency to be lost through
sedimentation. Several oceanographers, especially, R.C. Dugdale, R.W.
Eppley, and J.J. Goering, have pointed out that the flow of different
forms of nitrogen might serve to estimate the value of f, if it is
accepted that the recycling of nitrogen mainly affects ammonia compounds
(the form in which N is excreted by animals and other heterotrophs) and
that new production is based on the receipt of nitrogen in the form of
nitrate, proceeding from somewhere else, usually from below.

In stratified seas, or in the seasons when the water is stratified,
one can recognize a clearly defined level (often horizontally
discontinuous) just below the chlorophyll maximum that is considerably
enriched in nitrite. This is where the gradient of reduction in light is
strongest and the light becomes inadequate for photosynthesis, and where
nutrient concentrations suddenly increase (the nutricline). Here, the
planktonic algae that are settling pass through a zone where light is
insufficient for photosynthesis, but where they can absorb nitrate and
carry out the first stage of their chemical reduction (to nitrite).
Nevertheless, they do not have enough light to assimilate it and it
probably escapes, which would explain its accumulation at such a precise
level. One would expect the stratum with maximum nitrite to show greater
contrast when the f value is low.

2.4 The dynamics of phytoplankton production

Victor Hensen (1835-1924) who introduced the term plankton in 1887,
undertook a series of painstaking studies of the bay of Kiel. This was
the beginning of the quantitative approach to the study of plankton and
attempts to understand the environmental causes and interactions between
the different organisms involved in the dynamics of pelagic life. Hensen
also took part in the plankton expedition of the National (1889), the
first oceanographic expedition devoted to plankton and the beginning of
an overall quantitative approach to studying plankton (for the entire
Atlantic). Around this time, and even more so at the beginning of the
20th century, interest in understanding variation in fish populations
led to laboratories being set up in many coastal localities, such as
Ostend, Belgium (1843), Konk-kerme (Concarneau) in Brittany (1859),
Roscoff, also in Brittany (1871), Woods Hole in Massachusetts (1873),
and Naples, Italy (1874). One of their functions has always been the
study of local fluctuations in plankton populations, correctly
considered to be the basis of the fertility of the water. What started
off as keeping records of plankton changes led to a study of their
causes.

Variations in production in space and time

In temperate regions, at least near the coasts, a great abundance
of plankton--first diatoms, then copepods--can be observed in the spring
as the days lengthen and the surface waters warm up. In 1906 W. Natanson
realized that the increase in fertility was mainly due to deep
nutrient-rich waters rising up to the illuminated surface. The
commentaries on new production and recycled production, in the section
above, are fully applicable to the more stable situations that follow:
Marine blooms always occur in fits and starts whose origins are often
unclear.

Observations by the Norwegian oceanographers Haakon Hasberg Gran
and Trygve Braarud (1935), first off the coast of Norway and then in the
Gulf of Maine, showed the lack of uniformity in the spring plankton
peak, a discovery that led them to recognize the factors controlling
production. In very turbulent water whose nutrient content is uniformly
distributed throughout its depth, the phytoplankton increases first in
the shallower areas, where the seafloor places a lower limit on the
possible dispersion of plankton towards less illuminated levels. If the
depth is greater than 328 ft (100 m) and the water is very agitated, the
cells spend too little time under sufficient illumination to allow them
to reproduce indefinitely. These situations led to a delay in the
beginning of net production with a surplus. The greatest production
started as spring progresses and the light penetrates further, also
because this starts thermal stratification of the water that limits the
extent of vertical mixing. For production to take off, the depth of
mixing (measured from the surface) should not exceed a certain relation
to the depth of compensation--the depth where the production of the
system is equal to its respiration, and there is therefore no net
production. According to the Norwegian Harald Sverdrup (1953), this
limiting relation is between 1.5 and 5.5, depending on other local
circumstances. As this relation decreases due to increasing light and
reduction in the thickness of the highly stratified layer, the massive
production of phytoplankton gradually extends from regions nearer the
coast to deeper open waters.

This onshore view can be improved by contemplating what happens
from the high seas. The centers of the oceans have long been considered
especially barren: neither dense populations of diatoms nor schools of
fish ever develop there. The Sargasso Sea has always been the classic
example of this situation. However, relatively recent data have shown a
significant activity in which the minuscule organisms of the
picoplankton play an important role.

Production and upwelling areas

The situation is very different in areas of upwelling. Here, the
action of the winds, interacting with the direction of the coastal
currents and in conjunction with the forces associated with the rotation
of the Earth, makes the surface water flow away from the coast, to be
replaced by water from the depths, richer in nutrients. This is the
reason for their uninterrupted high primary production over long
periods. These areas have always been important fishing centers.

One can calculate the velocity of ascent of deeper water and the
quantity of nutrients it brings to the photic zone, as well as the
kinetic energy obtained from the hydrosphere-atmosphere system to carry
out the local mechanical work that supports this continuous high primary
production. This exosomatic energy is at least 25-50 times the light
energy involved in biological production. A similar relationship is also
found in terrestrial vegetation, where the exosomatic energy involved is
mainly in the form of evapotranspiration. In agriculture, it is also
necessary to include the additional energy used in irrigating,
fertilizing, and cultivating the soil. The application of the models of
ecological interaction formulated by Alfred J. Lotka (1925) and Vito
Volterra (1926) to plankton did not take place immediately, even though
Volterra was specifically inspired by a problem related to fish
production. The basic difficulty is that these models only sought to
describe the interaction between species, and between groups of species,
as entities abstracted from their setting, and they did not take into
account either spatial organization or external energy, both of which
are obviously very important in marine populations.

The water column model

Gordon A. Riley surreptitiously introduced space, by means of the
concepts of sedimentation and diffusion, the latter of which is
associated with the energy of turbulence. The conclusions of an
ecological approach to Atlantic plankton by Riley, Stommel and Bumpus
(1949) suggested a model according to which dF/dt = (r-gZ) F - V dF/dz +
Azd2F/dz2, where (if appropriate) we consider r-gZ = r'. In this
expression, F represents the phytoplankton, Z the zooplankton, V is the
speed of sedimentation (=0.001-0.02 cm per second), and A is the
coefficient of vertical diffusion, which is a measure of the turbulence;
z indicates that it refers to the vertical dimension. A, the first
letter of Austausch, or change, is a coefficient of diffusion,
expressing the transmission of heat, salinity, or movement in a liquid,
in g/cm per second (such as dynamic viscosity, divided by density, which
is approximately 1, the kinetic viscosity, expressed in [cm.sup.2] per
second). Plankton is scarce close to the surface, not because of
excessive light, but because of the discontinuity represented by the
surface of the sea, from which the plankton sinks but that it can only
enter by cell division. A can be calculated approximately by measuring
the downwards transmission of heat along a specific thermal gradient.
With reference to the vertical (Az) and the photic zone of the
Mediterranean, the values obtained are less than 2 between May and July,
from 2-5 in April-May and July-August, and higher than 5 between
September and April, when the waters are more agitated and more
productive. In the horizontal direction, Ax, it reaches much higher
values.

In the form proposed above, the model describes a vertical column
of water and cannot be directly applied to the real world where
horizontal differences, or those between different columns, are very
important. The physical structure of the sea is very complicated with
discontinuities that are almost as mobile as those occurring in the
atmosphere. This means that predicting changes in planktonic populations
is as difficult as predicting the weather.

Heterogeneities and asymmetries

The pelagic world contains a set of chemical reactions that take
place in a space that is progressively structuring itself, as happens in
some colloidal systems. In fact, ecological succession in pelagic
systems occurs in a medium that is becoming more structured or, at
least, is becoming progressively more thermally stratified.
Smoluchowski's (1918) considerations already suggested expressing
production (P) as dF/dt = P = AxC, where A continues to represent the
energy that is dissipated in turbulent mixing and C is the covariance or
degree of superimposition in the distribution of the factors of
production, basically chlorophyll, light, and nutrients. If external
recycling occurs, it should be considered as a ring that passes outside
the space of reference and joins imports (I) and exports (E). Thus, P is
the locally retained production: P + E = I + AC and P = AxC. In its
simplified form, without the recycling ring, this expression can be
derived with respect to time, giving:

[d.sup.2]F/[dt.sup.2] = dP/dt = C dA/dt + A dC/dt

which expresses succession rather elegantly, making it possible to
interpret how the decrease of available energy in diffusion or
turbulence is usually combined with a reduction of covariance in the
distributions of the factors of production. This decrease in the
covariance is equivalent to an increase in the segregation between
elements, an interaction that obviously contributes to production: The
tendency is always for nutrients to be depleted where there is light,
and so nutrients only accumulate where there is no light.

All the heterogeneities that arise show asymmetries. For example,
if eddies form that rotate in different directions, interference from
the rotation of the Earth leads to the breakdown of the initial
"impartiality" of any irregular mosaic, in the sense that the
centers of higher production associated with cyclonic eddies
(anticlockwise in the Northern Hemisphere) end up as isolated patches in
a background of lower production, and not the other way round.

Nowadays, structures of this type can be recognized in images
obtained from space. Oceanography has routinely included continuous
analysis and transects (temperature, salinity, and chlorophyll,
generally measured by fluorescence), on the basis of which we can
postulate a reasonable general two-dimensional structure into which we
can expect to fit and interpret the heterogeneities revealed by the
linear segments analyzed. The only compatible structure turns out to
consist of more productive, but discontinuous, patches, dispersed in a
background of lower productivity or biomass. These fertile patches
obviously, although not always, coincide with cyclonic vortices.

The logarithmic transformation of plankton concentrations X [x =
log (X + l)] along a transect makes graphs mosty symmetrical and reminds
us of the way that many of the distributions of plankton in space are
like the fractal profiles of mountain chains. If they are in two
dimensions, they show peaks that appear to be isolated or discontinuous.
These peaks, in our case, correspond to centers of high production from
which phytoplankton populations are dispersed. This is a very
generalized pattern in nature, and is surely the most common pattern in
the distribution of marine production in which local patches or
concentrations are always a feature.

Nowadays, computers offer many exciting possibilities that allow
the simulation of how plankton might multiply and evolve in accordance
with specific assumptions. It is natural that models of flows and
salinity, which show continuity, should be more acceptable than
biological models, in which history intervenes with all its uncertainty.
The scarcity of real data often leads to excessive interpretations that
are not always correct, bearing in mind the frequency of local
discontinuities and disturbances. The prospect for correct predictions,
on any scale, are still not very promising.

2.5 The processes of succession and biological types

Ecosystems never maintain the same organization for a long time. If
they maintain their activity within a reasonably stable environment,
they can always continue occupying space with slightly different (but
equivalent) structures that imply a lower maintenance cost, or by
enriching their own complexity without increasing the energetic cost.
Normally these changes are associated with the gradual consumption and
diminution of the quantity of nutrients available. This is the essence
of ecological succession (see volume 1, pp. 226 and following). In
plankton, succession shows the special characteristic, due to the
time-scale of the pelagic ecosystem, that all events and changes are
much faster than in benthic or continental ecosystems. This greater
speed facilitates the appearance of local differences.

Succession in phytoplankton

Succession in plankton never shows constant or uniform
characteristics between separate, even neighboring points. Normally,
local differences have been generated in time, either because changes
have occurred more rapidly in one area than another, or because
equivalent sequences have started at different times, depending on local
differences in the water turbulence, nutrient concentration, and the
distribution of light. Changes are always asymmetric: Gradual changes,
which are self-organizing and relatively slow, are interrupted by
sudden, random disturbances, usually accompanying an intensification in
the turbulent mixing of water or the displacement of water masses from
one level to another.

The dynamics of the plankton populations combine time and space.
More than once plankton blooms have been compared to clouds in the sky,
because the cells multiply most where there are movements of water of
the right strength and direction, which are especially effective when
they move nutrients closer to the light. However, all these movements,
whether they are unidirectional, like sea currents and upwellings, or
alternating and confused, such as turbulence, depend on external energy
that comes eventually from the Sun. Water is slightly less dense than
the organisms themselves, increasing slightly with increasing depth, and
receives light, heat and mechanical energy mainly at the surface level.
Growth will be intense while cells (or chlorophyll), light, and
nutrients coincide in space. Water tends to warm up on its surface and
stratify by density, and this acts against local vertical mixing. Mixing
is weak and may be caused indirectly, in association with horizontal
transport movements.

Excessively strong vertical mixing in deep waters means that each
cell of the phytoplankton, on average, enjoys light for too short a
time, leading to little or no growth and the excessive dispersal of the
population. If the thickness of the mixing layer exceeds by a certain
factor (between 1.5 and 5, depending on other circumstances) the
compensation depth (where biological production and respiration are
equal), there are too many losses and the plankton does not increase.
Even if conditions are optimal, the coincidence or high covariance in
the distribution of the factors or agents of productions soon decreases,
either because the population sediments and sinks to layers where light
is insufficient, or because of nutrient exhaustion, or more commonly for
all of these reasons.

A basic principle of planktonic life is that every atom of an
element that passes from the medium to the body of an organism will
probably return (from the same organism or another, such as a
planktophage or predator) to the environment, but at a lower level
(i.e., closer to the center of the Earth), than the level at which it
was assimilated. The net result is that there is a generalized downwards
transport of the elements in the water that are necessary for life. In
spite of temporary local ups and downs, the relatively stationary
situation reached is the result of interaction or interference between
biological processes and water movements. Normally the highest
biological activity is at almost twilight levels in terms of light
availability--at 131-328 ft (40-100 m) in depth. This stratum is only a
few meters thick and shows moderate biological production, stimulated by
the daily cycle of activity and by possible internal waves between the
upper fully illuminated and sterile level and the lower nutrient-rich
but dark zone. Since growth is controlled by the supply of nutrients, it
is not surprising that when the phytoplankton multiplies in the
twilight, it apparently makes poor use of the light that, in fact, is
available in excess.

The greatest quantity and activity of the phytoplankton is thus
located relatively deep, not because the surface light is noxious due to
excessive intensity, but because the surface of the sea, in addition to
being exhausted in nutrients, is a discontinuity from which organisms
sink but which they can only reach from below, and even then generally
only as a result of turbulent mixing of the water. In fact, most of the
light reaching the ocean is simply absorbed by the water and is of no
direct use to living organisms. It is understandable that the quantity
of chlorophyll that is found per square meter of ocean is, generally,
lower (often much lower) than that found in vegetation on the
continental surfaces. Normally, per unit area, this value is only 1/10
to 1/20 of that found in terrestrial vegetation.

For phytoplankton to produce, nutrients, light, and organisms must
occur together. Organisms are in general denser than water, and there is
thus an unstoppable flow downwards, although often slowed down by the
various mechanisms allowing swimming or passive floating, which is as
fatal as death for humans.

The return of the necessary chemical elements to the illuminated
surface waters and the continuation of the cycle of pelagic life depend
on external or exosomatic energy. Primary productivity, or phytoplankton
production, is proportional to the supply of necessary elements.
Phosphorus is the most important, then followed by nitrogen and others.
This seems to be the normal order, although it is possible that it may
vary locally and an element other than phosphorus may be limiting. It
appears that carbon is never limiting, or perhaps only locally, for
organisms that have evolved relying on a large excess of CO2 would be at
a disadvantage in excessively alkaline waters where most inorganic
carbon is present in the form of bicarbonate (HC[O.sup.3-]).

No situation can ever maintain itself stationary, persistent, and
uniform unaided. Nature in general, and the sea very clearly, moves in
fits and starts. Both storms and waves, whether superficial or internal,
introduce discontinuities on many different scales. These intermittent
influences affect the photic surface levels most, and these are the only
productive levels. Of course, there is a rich and varied life in the
abysses, supplied by the material that falls from the higher levels and
this manna falling from heaven does so in a way that is highly uniform,
given that it is made up of many small scattered episodes. These
episodes activate the photic zone irregularly, within a frame of time
and space large enough to allow the integration and evening out of the
flow of part of its net production on its way to the depths.

Swimming strategies

Each of the major taxonomic groups of phytoplankton has its own
"vocation" as a consequence of its fundamental characteristics
(for example, possessing ballast of opal or of calcite), or as a result
of an adaptive secondary evolution (the presence of different size of
appendages). Generally, the representatives of each particular group
live and multiply best--and are thus selected--under a specific set of
environmental conditions, or at particular stages of successional
sequences that are associated with respective productive episodes of
variable length, generally lasting from weeks to months.

If the surface water is nutrient-rich, production is fast and will
be even faster if the water is rising and the nutrients are continually
renewed where light is intense. In this situation, it is advantageous to
sink against the rising current, as this still maintains an acceptable
level of illumination. In calmer and poorer waters, cells do not divide
so fast and it is worth staying at the same level and increasing, as far
as possible, the capacity to absorb the little remaining food. It is
worthwhile devoting some energy to maintaining the cell in motion, using
flagella, and it is even better if these swimming movements lead to
vortices that increase absorption. This can be achieved by cell shapes
that might seem capricious to us, but clearly respect the laws of
hydrodynamics. These forms, possibly with small modifications, may also
play a defensive or dissuasive role against potential enemies.

The main biological types discussed below are stages in a sequence,
rather than discontinuous classes, although the divergent evolution
separating them may have included the need to solve some dilemmas.
Diatoms and coccolithphorids are immobile or only slightly mobile
organisms, with ballast, that can multiply rapidly and sink easily;
silicoflagellates might also be included in this ecological group. All
these organisms practise what in population dynamics is called an r
strategy. They multiply quickly, using the nutrients available at the
time, without concern for what might occur the future. On the other
hand, there are organisms, typically swimming organisms such as the
dinophytes (the ancient lords of the plankton) and other smaller groups
whose survival is due to their K strategy, where relatively low
reproductive rates combine with constant swimming and some other way of
surviving in a relatively resource-poor environment. Marine
phytoplankton is generally highly mixed, but relative alternation of
dominance by these two groups in time and space is worth noting.
Organisms with K strategies, especially the most diversified dinophytes,
can always persist in basically rich, fluctuating populations. As soon
as external conditions allow production to accelerate, the pre-existing
vegetation is joined by the result of rapid, often very local, blooms of
diatoms, coccolithophorids or Phaeocystis.

Regularities and variations

The pattern of change in the conditions of life may vary greatly
from place to place. Approximately the same situations may occur every
year and in sequences that correspond to the seasons: In the winter
there may be intense mixing of the water, shown by populations of
diatoms, while throughout the rest of the year the water is stratified
and the surface layer is almost depleted of organisms. These extreme
situations may show up to 10-fold or greater differences in production.

Irregularly distributed and rapidly varying phytoplankton blooms
encouraged by minor eddies (between 6-12 mi [10-20 km] in diameter and
generated by the local action of winds) often occur. If there are eddies
rotating in different directions, the cyclonic ones cause water to rise
in their center; they are more productive and usually contain more
diatoms, while the anticyclonic eddies are more passive. Another form of
circulation generated by the impulse of the wind takes the form of
narrow parallel bands (hundreds of meters long) called Langmuir cells.
They are often visible from airplanes, especially close to the coast,
from which they look like bands, hundreds of meters wide, with
alternating shiny and more opaque areas. The shiny areas show clear
surfaces, ascending waters, and more diatoms, while the more opaque
areas show descending circulation and a higher proportion of swimming
organisms.

Research transects across a region with many heterogeneous
structures give quantitative sequences that take the form of the outline
of a mountain range. They are compatible with a distribution consisting
of highly productive patches that are isolated and discontinuous, just
like typical cyclonic eddies, and dispersed over a background of lower
productivity.

Marine fronts are located on the edges of currents, or where
currents or water masses with different movements come into contact,
whether this movement is convergent, divergent, or involves lateral
sliding. When they meet they perform work and may provide nutrients.
These nutrients are often complementary, and this means that they are
the sites of higher biological production; as in more genuine upwelling
regions, they may contain blooms of coccolithophorids or diatoms,
possibly dominated by the latter. Tidal fronts, with mixed water, often
contain dense populations of coccolithophorids.

Situations of stratification may receive a continuous, often
horizontal, nutrient supply. This happens in bays or other coastal
systems with similar characteristics, often in persistently stratified
situations, caused by the advection or horizontal drag of the less salty
water. There swimming organisms sustain themselves (often multiplying
profusely), which may even give rise to "red tides" or
"red seas" in which toxic dinophytes are frequent. Some marine
regions are especially affected by these conditions, and this may have
been aggravated by the increasing flow of nutrients from land to sea.
This sort of episode usually ends in intense vertical mixing.

The distinction has often been made between neritic (or coastal)
plankton and oceanic (or open sea) plankton. The edges of the continents
interfere in the dynamics of the sea, especially in the coasts with
tides, and the energy of interaction produces a local mixing of water
and the corresponding local fertilization. This often leads to irregular
proliferations of diatoms that coincide with wind or sea movements that
mix the shallow waters. The study of situations of this type has helped
to clear up the basic mechanisms of marine primary production. We know
that the characteristics of the marine environment are very variable,
both in each volume of water and in the form of changes that take place.
There is a large number of organisms, many far removed from the general
behavior of the taxonomic group they belong to, which makes it difficult
to find regularities that are generally valid. Diatoms multiply rapidly,
but some species persist in cultures that are continuously illuminated,
while others do not thrive unless they are subject to a daily or
circadian rhythm of alternating light and dark. They also settle rapidly
and Riley, Stommel, and Bumpus, in their model for Atlantic plankton,
used a settling velocity for diatoms of 4-6 in (10-15 cm) per hour at
32[degrees]F (0[degrees]C), and twice that at 77[degrees]F
(25[degrees]C). Various other observations fall between 0.4-20 in (1-50
cm) per hour. Particular species have their own resources and escape
from being included in what might appear a general law. Oceanic diatoms
of large volume contain vacuoles with fluid that is lighter than
seawater, and which is maintained by the expenditure of additional
metabolic energy (such as the replacement of metallic cations with
ammonia).

During the summer, in surface waters, diatoms survive in
association with tintinnid ciliates. These function like outboard motors
maintaining Chaetoceros, and more rarely, Planktoniella in suspension.
Other diatoms (Thalassiosira) excrete strands of mucilage and make
masses that may also remain in suspension, or at least, change these
organisms' habitual form of life. Phaeocystis is another organism
whose cells are often covered in mucilage. Thus the fundamental
condition for phytoplankton production is the presence of nutrients in
the illuminated layers, or in other words, a high coincidence
(expressible by a covariance, C) in the distributions of light,
nutrients, and cells. The maintenance of the exosomatic energy necessary
for mixing to continue is provided by a measure of the turbulent
diffusion (A). Combining the two possible categories of both of these
descriptors allows the creation of a graphic with four compartments that
helps to sum up several aspects of phytoplankton biology.

The same diagram may be rotated through 45[degrees] to change the
coordinates, which then become respectively the quotient C/A and the
product AxC that now correspond better to stratification and
productivity. Using separate diagrams it is possible to mark the
statistical distances between different species, based on the
probability of these species coinciding in real samples of water. If a
simplified representation of this type is projected adequately on to a
C-A diagram as mentioned, it reinforces the meaning of this type of
representation, for which the name plankton mandala has been suggested.

3. The primary consumers: the zooplankton ********

3.1 The organisms of the zooplankton

Within marine trophic chains, zooplankton constitute the step that
channels the energy produced by autotrophic organisms to the secondary
consumers. To put it simply, the zooplankton make the energy generated
by the phytoplankton available to the large carnivores. Even so, the
role of zooplankton in marine ecosystems is much more complex, due to
its diversity of organisms and forms, and the range of strategies
followed by different species and groups. Zooplankton consists of all
the heterotrophic organisms--although some are known to be autotrophic
as a result of their symbionts--that live in suspension in the water
masses and depend on the water's dynamics, given that they lack the
ability to move.

Meroplankton and holoplankton

Although most zooplankton organisms are small, their actual size
range is between 20 micrometers and 7 ft (2 m). Among the smallest are
the flagellates, while the largest include the jellyfish and
siphonophores. Leaving to one side formal classifications based on size
and zoological groupings, it is important to distinguish between two
different types of zooplankton organisms: those that pass all their life
in the plankton (holoplankton) and those that only colonize the pelagic
environment at some stage in their life cycle (meroplankton). This is
the case of the larval phases of many organisms, such as sessile or not
very mobile benthic organisms, that use the pelagic medium to disperse
themselves. The larvae of fish and many species of benthic decapod
crustaceans, for example, develop entirely in the plankton.

During their period in the planktonic medium, the organisms of the
meroplankton pass through different stages of morphological
transformation until they reach their juvenile phase, very similar in
form to the adult. How long the larval phases reside in the plankton
varies greatly depending on the species, but for all of them it is the
most critical period of their life cycle. In addition to the larvae of
decapod crustaceans mentioned above, other groups of benthic organisms
contribute in the same way to the zooplankton communities. Among the
most important are the larvae of echinoderms and the medusa phase
(polyps) of many benthic cnidarians, as well as those of many fish.
These larval stages reside in the plankton for a period that varies
between weeks and months, and for short periods of time, may represent a
high percentage of the zooplankton biomass of coastal systems. Many
other groups of benthic animals, such as sponges, polychaetes, and
bryozoans, also produce a large number of planktonic larvae during their
period of sexual reproduction. Unlike the groups mentioned above, the
larvae of these animals only remain in the plankton for a few hours or
days and undergo their first metamorphosis as soon as they have found a
substrate to become established. The mortality of these larvae is
enormous; they take advantage of the planktonic medium to disperse, but
have to pay the high price of forming a very important seasonal source
of food for other organisms of the coastal zooplankton.

Although the meroplankton may be an important component of
zooplankton communities, most of the biomass of these communities
consists of holoplankton. Copepods are by far the dominant group,
forming 50-90% of the individuals in these communities, and their
biological cycle takes place entirely within the plankton. The highest
percentages of copepods have been found on the continental platforms in
the northern half of the Atlantic Ocean, with the lowest in the tropical
areas of the Indian Ocean. With respect to biomass, in the North
Atlantic copepods represent slightly more than 50% of organic carbon in
oceanic areas and nearly 75% in coastal areas. This difference in
biomass is largely explained by the presence of large oceanic
populations of euphausiids (krill), which can account for more than 30%
of the zooplankton biomass. The tendency observed in the North Atlantic
is repeated in other oceans, although in the tropical areas of the
Pacific and Indian oceans the biomass of krill is greater, and in
addition, other groups, such as amphipods, chaetognaths, cnidarians, and
pteropod mollusks each represent about 5% of the total biomass. These
figures generally underestimate the biomass of gelatinous zooplankton,
formed by jellyfish, siphonophores, ctenophores, pteropod mollusks, and
thaliaceans or salps. These gelatinous organisms are not collected
efficiently with the normal sample nets used for zooplankton because of
their large size and the fact that they form dense accumulations or long
colonies. Recently it has become possible to assess both their biomass
and activity in some areas. In addition to being very abundant, some
gelatinous zooplankton (especially large medusas) are voracious
carnivores, competing with fish larva as predators of the small
zooplankton.

The trophic structure of zooplankton is clearly dominated by
macroherbivores (filter-feeders and browsers) and omnivores (in reality
herbivores able to eat small inert particles and tiny organisms). In
temperate and polar areas these two represent more than 70% of the
zooplankton biomass. In tropical seas there is a notable abundance of
predators (carnivores) that represent nearly 40% of the total biomass.
These trophic differences are related to the lower phytoplankton biomass
and production of tropical seas, caused by their poverty in nutrients.
Near coral reefs herbivores represent less than 10% of the total
biomass, as phytoplankton are scarce because reefs act as nutrient
traps, developing a rich flora of endobionts and symbionts.

Seasonal variations

The values given above refer to an annual mean. However, as in
terrestrial ecosystems, marine ecosystems show seasonal variations, and
these increase with distance from the equator. This temporal variation
is shown by an oscillation in the number of species and individuals,
basically caused by changes in activity related to modifications in the
hydrographic conditions of the water column.

In temperate seas, zooplankton show two periods of maximum
abundance, one in the spring and the other at the end of summer. Cold
seas only show one peak, in the summer. In tropical areas zooplankton
concentrations are constant throughout the year. The peaks of abundance
respond to a hydrographic model in which, when the number of hours of
light increases, the photosynthetic activity of the phytoplankton also
increases, making use of the nutrients from the previous winter.

The increase in phytoplankton leads to an immediate response by the
herbivorous zooplankton. This mainly consists of copepods, which consume
20-30% of the daily primary production. Continuous browsing by copepods
gives rise to a biomass peak in the spring, made up of larger
individuals than during the rest of the year. They can grow quickly and
reach sexual maturity in a few days. Their life expectancy is about 20
days and for the last 10 they ceaselessly lay eggs.

The females of some species lay hundreds of eggs a day, although
production decreases at the beginning of spring, as a result of the
depletion of nutrients, and thus phytoplankton. In general, production
by herbivorous zooplankton is very rapid and the biomass of zooplankton
can increase by 10 times that of winter concentrations. The success of
the copepods is largely because their metabolism allows them to grow
very quickly. They invest more than 33% of the energy they absorb in
growth and reproduction, and the degree of assimilation of the food they
capture is nearly 60%; they are thus very effective when food levels
permit.

One should also note that in warm seas during the spring, in
addition to herbivorous copepods, there may be high concentrations of
salps (Salpa), which are able to consume more than 40% of daily primary
production, especially when they form dense swarms. These swarms can
clog fishing nets, which may gather several tons of these organisms in a
few minutes' trawling. As they form colonies of many individuals,
the salps can compete effectively with the copepods for their common
food. The copepods may reach densities of 5-10 individuals per liter,
while salps may exceed 20 individuals per liter.

Many carnivores, ranging from copepods to large jellyfish and fish
larvae, increase at the same time as the herbivorous zooplankton peak.
The activity of the carnivorous zooplankton does not prevent herbivores
from exploiting the phytoplankton effectively, or the phytoplankton from
exhausting the nutrients. As zooplankton activity increases, the summer
warming of the surface waters leads to increasing stratification. This
change in hydrographic conditions and the activity of the organisms both
lead to a diminution in the abundance of the zooplankton. In autumn, sea
level winds help break up the summer thermocline, making nutrients
available to the phytoplankton by once again suspending all the organic
material generated during the summer, which was largely trapped below
the surface layers by the thermocline. This leads to a second peak in
zooplankton concentration consisting of smaller, very active, and
efficient herbivorous copepod species (less biomass than in the spring)
and a peak in production. Later, when winter arrives, falling
temperatures and shorter days considerably reduce phytoplankton
activity, leading to a corresponding reduction in zooplankton biomass.

In warm seas there are large-scale phenomena of seasonal variation
in zooplankton biomass and diversity. These are similar to those
described for temperate seas, although they depend on factors other than
thermal variations, which are very moderate in tropical areas. An
important difference is that in tropical seas they are local and occur
more frequently close to the coasts, whereas in temperate seas seasonal
zooplankton variations may occur anywhere. Large-scale meteorological
phenomena are a good example of this, such as the seasonal changes of
the monsoon regime in the Indian Ocean. For almost half the year, the
prevailing winds are persistent and blow from sea to land, and during
the other half of the year they blow in the opposite direction. When
they blow offshore, surface water is displaced towards the high seas
compensated by upwelling of deep, cold, nutrient-rich water that causes
a period of great abundance of zooplankton. During this period the
community is dominated by species whose life cycle occurs in coastal
areas with a large meroplankton component. On the other hand, when
onshore winds blow from the open sea, the zooplankton community is
dominated by oceanic species, and productivity decreases as the deep
layer is trapped under the photic layer. An example of this type of
seasonal variation is found in the species composition of the population
of hydrozoan medusas on the eastern coasts of Papua New Guinea. During
the period of offshore winds, most species undergo a benthic polyp phase
that produces many small planktonic medusas. These medusas stay in the
plankton for a few weeks, until their larva, the result of sexual
reproduction, return to the seafloor. During the period of onshore
winds, however, the community is dominated by larger medusas whose life
cycle takes place totally in the plankton, where they remain for several
months.

The far more intense genuine monsoons generate important,
large-scale seasonal differences in the zooplankton of warm seas.
Monsoons are periods of torrential rain, during which rivers discharge
large quantities of water on the continental platform. The high
concentration of transported nutrients in this water rapidly starts a
cycle of biological production favoring the development of dense
populations of herbivorous zooplankton. The length of the monsoons means
that these continental inputs are continuous, and so succession in the
planktonic ecosystem allows the proliferation of a large number of
carnivorous species and other secondary consumers, although they do not
attain the level of structure and complexity observed in temperate seas
during the spring.

Support systems

The zooplankton contains animals that live in continuous suspension
in the water, but with a limited capacity of movement. Most marine
activity and production takes place in the top (656 ft [200 m]), so the
main strategy of zooplankton is to prevent themselves from sinking. To
achieve this, they have either developed morphological modifications or
perform some sort of activity that keeps them afloat. One of the most
common adaptations is having a range of appendages or body extensions,
increasing their surface and offering more resistance to sinking in the
water column. This also reduces the need to move continuously, and thus
the metabolic expenditure it represents. There are many examples of this
strategy, such as the expansions of echinoderm larvae, the appendages
and prolongations of decapod crustacean larvae, molluskan parapodia and
the feathery appendages of many crustaceans.

One alternative strategy is the inclusion of low-density fluids,
globules of oil, or even small gas chambers within the body. Fish eggs
contain diluted fluids to ensure their buoyancy; otherwise they would
rapidly sink to the bottom, as they are spherical and lack any locomotor
ability. Siphonophores have gas-filled spheres in the upper zooid of the
colony that maintain them permanently and almost effortlessly in
suspension. Many euphausiids and copepods contain oily inclusions in
their adipose tissues that, together with their capacity to move, helps
them to float. Gelatinous phytoplanktonic organisms (jellyfish,
siphonophores, ctenophores, pteropod mollusks, salps [thaliaceans]) can
change the ionic balance within their tissues and so regulate their
buoyancy. Some siphonophores and other organisms, such as the
dinoflagellate Noctiluca, contain cavities with iso-osmotic solutions of
ammonium chloride that they can regulate to improve floatability.

A large difference has been observed between species whose
adaptations include bodies with almost neutral buoyancy (meaning they
need exert almost no effort to maintain their level), and those forms
whose structure forces them to swim continuously to prevent themselves
from sinking. Thus, for example, the chaetognaths of the genus Sagitta
need only swim from time to time to maintain themselves at the desired
depth, while mollusks of the genus Cavolinia have a heavy shell and must
swim vigorously with their wing-shaped appendages to prevent themselves
sinking. In general, organisms living in tropical waters (which are less
dense and viscous than temperate and polar waters) are smaller and have
more appendages and projections than species in other seas.

3.2 The distribution of zooplankton

The distribution of zooplankton depends mainly on the movements of
water on a global scale. Although the oceans are interconnected, complex
ocean currents and macro-scale and meso-scale hydrographic structures
mean that very few zooplankton species have a worldwide distribution.
Species that do have a worldwide distribution have had to follow a long
process of dispersion and adaptation since their appearance, overcoming
hydrographic obstacles, such as areas of convergence and divergence, as
well as large-scale currents, such as the Cromwell Current (186 mi [300
km] wide), which circulates eastward under the equator at a speed of
three knots.

Zooplankton are suspended in different masses of water and adapt
their physiology to its hydrographic characteristics, as well as to its
specific values of temperature and salinity, and thus density. The
adaptation of different species to a specific water mass gives rise to a
very heterogeneous pattern of distribution because of the wide range of
different bodies of water that may be found within a single ecosystem.

The adaptation of zooplankton communities to specific water masses
responds to the classic view, contested by more recent ideas, that
attributes a predominant role to hydrodynamics in explaining large- and
medium-scale zooplankton distribution. It might be that the dynamics of
water gives rise to the mechanisms that create heterogeneity in the
distribution of planktonic organisms.

Zooplankton distribution is not only influenced by environmental
factors, but also by biological factors resulting from their activity,
morphology and physiology. Zooplankton distribution is heterogeneous in
both space and time. It is generally, though not universally, accepted
that spatial variability is due to physical factors, while temporal
variations are due to biological factors. Much has been written about
this controversy, although in reality both types of factors are
interrelated in each particular area, and the preponderance of one of
the two factors depends on the scale at which the phenomenon are
observed.

Oceanic-scale distribution

On a large scale, ocean currents and cyclonic gyres mark the limits
of the biogeographical regions of the different planktonic fauna. In
areas where these types of currents meet, frontier zones or currents
develop and physically limit the distribution of species. In the
southern hemisphere, the confluence of the Benguela Current and the
Agulhas Current (from the southern Indian Ocean) on the western coast of
southern Africa gives rise to an area of divergence that acts as a
frontier between the faunas of the South Indian Ocean and the Atlantic
fauna. Oceanic-scale areas of convergence-divergence, such as the polar
front in the southern hemisphere, act as natural frontiers preventing
species from entering the Antarctic Ocean and Antarctic species from
leaving.

Intermediate-scale distribution

Heterogeneity in space and time on an intermediate scale in the
zooplankton (between approximately 6 and 62 mi [10 and 100 km], and
between three months and 15 days) is governed by a series of more or
less persistent hydrographic structures that cause dispersion and
concentration. As mentioned before, zooplankton does not show a uniform
distribution, but tends to concentrate in certain areas, where
hydrographic phenomena on the most suitable scale occur. It appears to
be evolutionarily positive that different species should have adapted
their biology to the existence of more-or-less permanent hydrographic
variability, as this means they can live together in the same marine
system without dispersing very much. The organization provided by the
spatial framework is of vital importance for the maintenance of the
marine foodchains, in which the investment in seeking food cannot be
greater than the returns provided by the food that is found.

Advective processes

Advective processes are among the best-known mesoscale hydrographic
phenomena. The currents that regularly displace bodies of water over the
continental platform are responsible for the zooplankton gradients along
coastal zones. For example, the continuous nutrient-rich incursions of
the California Current are the cause of the area's year-to-year
variations in zooplankton biomass and change the structure of the
zooplankton community by increasing the quantity of herbivores
associated with the southern tip of the current. The proliferation of
herbivorous zooplankton will lead to an increase in the populations of
carnivores off California. In this way variations from one year to
another in intrusions by the current determine the supply of prey for
fish larvae and affect the growth of the annual populations of
commercially important fish species.

The impact of advective processes on local zooplankton communities
is not always so positive. For example, when there is a diminution of
the upwelling in the north of the Benguela system, warm water enters
from the Angola Current. These waters bear many medusas and
siphonophores, which are such voracious predators that they may have
negative effects on the rest of the area's zooplankton. In fact,
the low concentration of copepods in the north of the Benguela Current
(one third that observed to the south during the relaxation of the
upwelling into surface waters) is thought to be due to the high
predation by what is known as the gelatinous zooplankton present in the
intrusions from the Angola Current. In other cases, such as off the
coasts of Oregon and Catalonia, the displacement of a current parallel
to the coast tends to mark the spatial limit of the platform zooplankton
communities. Thus, the zone situated between the coastline is
characterized by a zooplankton that rarely strays far from the coast,
while on the other side of the current the community that develops is
dominated by holoplanktonic species. Between them and associated with
the current, there is a typical platform community that acts as a
transition between the coastal and oceanic communities. Slackening of
the current will allow meroplanktonic species to penetrate nearer to the
coast, increasing species competition or leading to the dispersal and
possible loss of coastal species.

A further type of advective process that is of great importance for
zooplankton are the intrusions of continental waters from large rivers
like the Mississippi. High nutrient concentrations make these inflows of
water productive and are highest at the tip of the intrusion, where
large agglomerations of zooplankton serve as food for fish larvae, whose
population increases in accordance with the quantity of materials
provided by the river.

Internal waves

Internal waves are also a source of variability in zooplankton
communities. The flow of currents over the continental platforms and the
relief of the seafloor together generate a series of internal waves
associated with nutrient concentration phenomena and an increase in
primary production. At the same time they act as transport waves
favoring local concentrations of zooplankton. Their importance is
clearly shown, for example, by the way some populations of decapod
crustacean larvae move along the coast by the stratum closely associated
with these internal waves, taking advantage of the food concentrations
to survive and go through metamorphosis.

Fronts

Hydrographic fronts act as areas of convergence, creating an
important discontinuity in the horizontal distribution of water masses.
They are associated with high plankton production, which gives rise to
an increase in the production and biomass of zooplankton. Thus, fronts
act as zones of accumulation as well as areas of zooplankton retention
and transport. Along the front water rises and falls, thereby keeping
the organisms close to the surface and preventing nutrient sedimentation
by causing mixing processes. Localized fronts in the Ligurian Sea or in
the North Sea show concentrations of copepod larvae that are much higher
than the surrounding waters. In a front in the English Channel,
concentrations may reach 75 times greater than the "normal"
values for the surrounding coastal waters. This provides an ideal
habitat for the proliferation of a rich carnivorous zooplankton, such as
fish larvae.

While oceanic frontal systems act as zones of retention, those of
the platform and slopes also act as barriers to dispersal. In a front
located at the end of the continental platform in the western
Mediterranean, large agglomerations of the larval forms of fish whose
adult forms live in coastal waters have been observed. The larvae of
these species might be dispersed towards the open seas, but the platform
and slope fronts prevent their loss and encourage their later
settlement. Many larvae of mesopelagic species are also associated with
the front, thus increasing interspecific competition for food, but
possibly solved by the high rate of plankton production associated with
the front. As in other platform and slope fronts, the current
circulating on the ocean side is responsible for the formation of the
front, in which the waters of the platform collide with those of the
slope. Therefore, this hydrographic barrier effect limits the dispersal
of the zooplankton of the platform.

Tidal and estuarine fronts are also associated with greater
plankton productivity and biomass than in surrounding waters. For
example, in the Georges Bank, a tidal front acting as a barrier has been
shown to prevent dispersal of planktonic species to the exterior.
Furthermore, the external part of this front shows a high associated
zooplankton biomass, which enters the interior of the bank by means of a
compensatory bottom current. This current associated with the front is
very important because it supplies the food needed to maintain the
populations of icthyoplankton, vitally important for maintaining stocks
of the locally exploited species of fish. In some estuaries on the
eastern coast of Canada, it has been shown that there is a
synchronization between the existence of an estuarine front and the
development of the population of fish larvae. The front moves towards
the exterior of the estuary, and many larvae are associated with the
zones of mixing. Towards the interior of the estuary the larvae are very
small and feed on copepod nauplius larvae. As the front reaches the
mouth of the estuary, the larvae are found to be larger and feed on
small copepods and then, eventually, on adults. The feeding adaptation
of the larvae through increase in size ensured resources were not
exhausted before the end of development.

Winds

The western coasts of continents show a regime of winds that favor
the upwelling of deep water. These upwelling waters are so rich in
nutrients that they are the starting point for productivity high enough
as to place them among the most productive areas in all the world's
oceans. The zooplankton respond by producing dense populations of
opportunistic species, mostly herbivorous, resulting in communities that
are little diversified and are dominated by calanoid copepods. The
system can support a large biomass of zooplankton, the basis of the food
supply of secondary consumers (fish and cephalopods).

The displacement of the surface bodies of water towards the open
sea generates the divergent Ekman flow, used by many fish larvae to
leave coastal areas. This displacement may, however, have negative
effects because it removes the larvae from production centers. The
solution adopted to avoid this forced transport has been the development
of vertical migration, which situate individuals below the layer of
water being displaced when the winds blow from the land to the open sea.
On the coasts of Namibia and Peru it has been observed that when
upwelling weakens, zooplankton communities become more complex as the
number of species increases and the number of individuals of the
dominant species falls. At the same time, the more opportunistic species
of copepod are replaced by species with slower potential growth rates
and lower egg production. The densities of copepods in the Benguela
upwelling range from more than 4,000 individuals per cubic meter in weak
upwelling to more than 12,000 when upwelling is strongest.

Currents

Very strong currents often produce a series of lesser divergent
currents that displace large water masses to the exterior of the central
body of the current. These water masses form eddies that encircle a
zooplankton community similar to that in the current they originate
from. These eddies are surrounded by other bodies of water with very
different zooplankton communities. The continuous circulation of eddies
means that their zooplankton community can maintain itself close to the
surface and evolve. After a time, organisms from the surrounding water
masses penetrate the eddy's interior, thereby mixing and changing
the community's structure.

The development of isolated communities of plankton has been
studied in eddies created by the Gulf Stream that may persist for
several months. Similar structures--such as the rings or circles of warm
water associated with the Kuro-Shivo Current or that to the east of
Australia--act as minisystems maintaining very specific zooplankton
communities in isolation for a certain period of time. The many species
within these hydrographic structures develop almost without contact with
the exterior. It has been observed that eddies in waters around Hawaii
include a large number of fish larvae of species whose adult form is
found in coral reefs. These larvae flee from the habitat of their
progenitors because adult fish of the same species are the main
predators of the larvae. They grow within the eddies until they reach
the juvenile stage, and then they return to their adult habitat to
gather. These retention mechanisms are considered very important in
ensuring larval survival, since within the eddy they have easier access
to more concentrated food resources than in the exterior, where
organisms are more dispersed.

Other processes on a meso-scale contribute to increasing the
zooplankton's heterogeneity in space and time. Phenomena such as
residual currents associated with eddies or fronts, the formation of
discrete layers of plankton accumulation, and circulation within marine
canyons, all introduce variability into the mesoscale distribution of
zooplankton. In the submarine canyons of the Georges Bank, for example,
euphausiid density is high (more than 1,000 individuals per square
meter). This helps to explain the area's high production, as the
zooplankton biomass of the interior of the bank and its production do
not explain how the needs of the fish population are met. The discovery
of these dense concentrations of crustaceans, associated with the bottom
currents of the bank's submarine canyons, closes the productive
cycle.

Small-scale distribution

Although meso- and macro-scale variability in the distribution,
abundance, and production of zooplankton is mainly governed by
hydrodynamic processes, it seems that on a small scale biological
factors acquire greater importance. There is, however, a series of
physical phenomena related to the formation of convection cells, or
Langmuir cells, that may influence plankton distribution on a small
scale 33-328 ft (10-100 m).

The factors that influence distribution

Heat loss from the surface water produces an increase in its
density. Therefore, during the night it sinks and is replaced by warmer
water from below. This generates convection cells, with water sinking
and rising. Organisms with positive buoyancy can locate themselves in
convergence areas, taking advantage of the rain of food from the
surface. Organisms with negative buoyancy will tend to be in the
divergence areas, while those with neutral buoyancy may concentrate at
the base of the cell or at the surface. This physical support for the
distribution of plankton favors the tendency of each species to
aggregate in order to occupy the most suitable space. The heterogeneity
achieved is quite varied, as a convection cell may range from a few
meters to almost 656 ft (200 m) in size. However, factors related to the
social behavior of species, their demography, life cycles, and
intra-specific relations all play essential roles when it comes to
explaining small-scale distributions.

The level of heterogeneity (variation in the number of species or
of individuals) found in a horizontal kilometer is about the same as
that found in roughly ten vertical meters. Most zooplankton organisms
tend to concentrate in the top 656 ft (200 m)--the photic zone or a
little below. For example, on the continental Atlantic platform of North
America average annual zooplankton biomass in the first 164 ft (50 m) is
199 [cm.sup.3] per 1,000 [m.sup.3] of water; between 164-328 ft (50-100
m) it is 94 [cm.sup.3]; 35 [cm.sup.3] between 328 and 656 ft (100 and
200 m); and below 1,640 ft (500 m) it is lower than 20 [cm.sup.3] per
1,000 [m.sup.3] of water. These differences in zooplankton biomass are
less pronounced in other areas, such as the Sargasso Sea or the Gulf
Stream, but biomass values in the top 328 ft (100 m) are always at least
double those found at 656 ft (200 m), and ten times greater than those
found at 1,640 ft (500 m). Parallel to this greater abundance of
zooplankton in the surface layers, there is a pattern of vertical
displacement by organisms that is the result of an environment which is
more active than the rest of the oceans.

Swarms of organisms

The tendency to live in groups, forming single-species patches or
clouds, is a common strategy among zooplankton organisms. Causes leading
to aggregation include differences or gradients in salinity and
temperature, gradients of light intensity, the distribution of food
resources, the presence of predators, and social behavior. The size of
the patch or swarm depends on the species, and the size of the
individuals varies with external factors and also during their
development. For example, in copepods the swarms of nauplius larvae are
generally larger than the swarms of adults, possibly because there is a
larger number of individuals in the swarm. At the same time, a swarm of
adults may increase if it finds an accumulation of food, or decrease if
it detects the presence of a predator. Thus, swarms function like an
accordion and fluctuate in size.

The size of the zone where a species occurs may fluctuate during
the day, over its development, or depending on the areas where it is
found. A species may show phases of aggregation and of dispersal. This
fluctuation in distribution makes it difficult to assess population
density using conventional methods (nets or suction pumps). The density
at the center of a copepod swarm is 100-1,000 times greater than the
average density of the total population of the area. Furthermore, the
role of prey or predator in the trophic relationships of the community
changes greatly depending on whether the copepods are grouping or
dispersing.

The advantage or adaptive value of swarm formation is still hotly
debated. If we look at a swarm of sardine larvae, we will see that the
individuals at the center of the swarm are very well protected from
predators: They are, however, relatively isolated from the food supply
on the edge of the swarm. One option is to remain together during the
day to avoid predators and disperse at night to feed. In general, and on
the scale of a system, the formation of aggregations facilitates the
distribution and recycling of available energy. Solitary individuals
have to displace themselves continuously to capture prey, and it is also
unlikely that they will be captured, so there are many possibilities
that they will be lost to the trophic chain (at least in the top 656 ft
[200 m]). Zooplankton excreta contains vital nutrients for the
phytoplankton. Products excreted by swarms are easier for algae to
capture because they are much less dispersed than those produced by
isolated individuals.

The characteristics of a swarm or aggregation vary greatly from
species to species. However, if we compare two species of copepod,
Calanus finmarchicus and C. tonsus, we can see that their behavior is
different. C. finmarchicus forms swarms that last between 12 hours and a
few days, which then break up and reform again a few days later. These
swarms are between 3-10 ft (1-3 m) in diameter, with a density of more
than a million individuals per cubic meter. C. tonsus forms swarms
ranging from 328 ft to 0.62 mi (100 m to 1 km) in diameter, with a
density of 10,000 individuals per cubic meter. The average distance
between the individuals in a single swarm varies greatly. In copepods it
may be less than 0.4 in (1 cm), while in euphausiids it is from 1-2 in
(3-5 cm), and in large medusas it may be 39 in (100 cm). Studying
copepod swarms living on coral reefs has shown that a single group may
form swarms with different characteristics. They form dense
single-species aggregations about a cubic meter in volume just above the
surface of the coral colonies with densities of more than half a million
individuals per cubic meter. There are even swarms consisting of
individuals of the same size but of different species, showing no social
relationship. Other swarms may show social behavior, as many fish do.

The swarms of a single species show a differentiated demographic
composition. For example, in aggregates of medusas like Ropilema
sculentum (with an umbrella 8-16 in [20-40 cm] in diameter) the
individuals of the same size are grouped by their ability to swim,
forming a group of swarms within a larger swarm. All the different
swarms move together to find food, at a speed of about 656 ft (200 m)
per hour. In many species, swarming was originally reproductive. All the
individual members of a swarm were produced at the same time by an adult
population. For example, the adults of a swarm of sardines all lay their
eggs at the same time, so the eggs form a single aggregate at the mercy
of the currents. As the individuals grow, the swarm loses a part of its
population, especially those on the periphery, while the others continue
together until they reach the juvenile, or even adult, stage.

3.3 Vertical displacements of zooplankton

Vertical displacement of zooplankton species is due to various
causes, although light is the factor that appears to trigger migration.
Vertical migrations may also have an ontogenetic component, as swarms of
larval, juvenile, or adult forms of a single species may follow
different migration patterns. Although adult chaetognaths move
throughout the water column, juveniles form swarms at very specific
depths, close to the level where the swarms of small copepods they prey
on are most abundant.

Migratory movements

Most species rise to the surface during the evening or night, and
descend when the new day arrives. As has been shown for some species of
copepod and other crustaceans, very slight changes in light intensity at
the surface cause an increase or decrease in displacement, depending on
the frequency of the stimulus. Some types of obstacles that cast a
shadow on the receptor organism also stimulate vertical displacement.
Although most migrations take place in the upper layers of the water
column, they are also habitual in organisms that live below 1,640 ft
(500 m) depth. The difference is that in the photic layer the rhythms of
activity are very short, because they respond to the day-night cycle,
while at greater depths the slower rhythms of migration last a few days.

The speed and intensity of vertical displacement depend on the
group and the hydrographic conditions of the geographical area.
Medium-sized copepods, for example, can rise 98-197 ft (30-60 m) in an
hour, while euphausiids can rise 328-1,312 ft (100-400 m) in an hour.
Some more littoral species, such as the larvae of the acorn barnacles of
the genus Balanus, only rise 49 ft (15 m) in an hour, although for this
organism it is important for the larvae not to stray too far from the
habitat of the adults because, if they migrated large distances, they
would be swept away by currents. Descent, using gravity, may be faster
with the consequent advantage of escaping from predators. Furthermore,
in many species migration may be inverse, that is to say, descending at
night to evade predators.

Food migrations

Migration represents a certain metabolic cost, compensated by the
benefits it provides. The evolutionary meaning of migration is based on
the relevance of these benefits. On the one hand, displacement within
the water column is related to the search for food. Many copepod
populations are found below the level of maximum chlorophyll and rise to
eat during the night, while other species remain at the surface where
they graze on the phytoplankton. The migration of copepods leads to a
synchronous displacement of their predators, in search of rising or
falling swarms. Many predators, such as fish larvae, hunt visually and
so during the day their prey migrate towards less illuminated areas,
making them harder to locate. Many researchers consider migration as a
strategy to escape predators. A different, metabolic, explanation is
that copepods produce a larger number of eggs in warmer surface waters
and show higher growth rates. In deeper, colder waters their metabolism
and growth rates are slower.

All researchers agree that migration is governed by a set of
intimately related biological factors. The following is a typical
explanation of migration. A swarm of a particular species of copepod
that occurs at 328 ft (100 m) depth during the day, starts to move
towards the surface when the sun sets. The swarm displaces in a regular
way, so that the individuals at the top remain at the top. When they
reach the layer of maximum density of phytoplankton, they begin to graze
continuously, and the individuals that are satiated begin to descend
while the other members of the group rise. At dawn, the population
descends rapidly, with stomachs full of algae that make them visible to
predators.

While at the surface they eat and excrete continuously, and because
their metabolism is faster, they also produce a larger number of eggs.
In fact, egg production occurs mainly at night, as has been observed in
the copepod Acartia pacifica in the Sea of Japan. During the day
production is about 30 eggs per cubic meter per hour, while at night it
is about 150. Once they have reached the colder layers they reduce their
movement and, as their metabolic activity decreases, they spend their
time digesting the prey captured during the night.

Defensive migrations

Many zooplankton organisms, such as chaetognaths and medusas, are
transparent and during the hours of light they are almost invisible to
their predators who hunt by sight, and so they can stay at the surface.
But when they eat, the prey ingested makes them visible to predators,
and they have to leave the illuminated surface zones. They go down to
darker layers where the temperature is lower, and where they can digest
their prey more slowly and wait for the night or the following
day--depending on the speed of digestion--before rising to hunt again.

There are many species that in certain circumstances do not
migrate. If a predator is in an area with sufficient prey, then it need
not migrate and thus saves the costs it would represent. If the center
of the swarm coincides with an adequate concentration of available food
and no predators are detected nearby, the swarm opts not to move.

Migratory obstacles

Apart from trophic circumstances, physical factors also alter the
migration of many species. The existence of a clearly formed thermocline
may act as a barrier to migration. An example of the action of the
thermocline is the vertical distribution pattern shown by zooplankton
groups in the north of the Benguela ecosystem. In this area the
intrusions of hot water from the Angola Current give rise to a strong
thermocline of about 43[degrees]F (6[degrees]C), at a depth of about 164
ft (50 m). Many species of medusas, chaetognaths, and amphipods
concentrate just above the thermocline. The high concentrations of
copepods at the surface throughout the daily cycle and the high cost of
crossing the thermal discontinuity of the thermocline, are the reasons
why some species do not move, or only perform short movements between
the thermocline and the surface.

Migratory strategies

One way in which a plankton community gains from migration is
related to copepod excretion. They release their excrement in the upper
layers in the form of fecal packets, contributing to nutrient
remineralization, because bacteria close to the photic layer can
decompose the products of defecation as they fall.

Flagellates are also important and in addition to showing
heterotrophic nutrition, like most protoctists, they also possess
pigments that make them autotrophic. Zooplankton organisms that ingest
these protoctists manage to increase the yield of the planktonic trophic
chains by more than 50%.

The fact that most species of the plankton zone are concentrated in
the photic layers raises the question of density dependence. This
implies that the different species spread out--often by migratory
movements--within the water column, occupying levels that are often
highly discrete. For example, studies of the vertical distribution of
some species of copepod in the Black Sea showed that each species
located the center of its population at a specific depth. So Acartia
clausi was 30-36 ft (9-11 m), Paracalanus parvus between 13-16 ft (4-5
m), and Oithona nana was between 16 and 36 ft (5 and 7 m) deep.

Density-dependent problems also arise in competition for food. For
the larvae of different fish studied on the coasts of Britain, one
solution was to select the type of prey according to size and to the
level of distribution of the different species. Thus, one species
specialized in the predation of one species of copepod, while other
larvae ate small copepods of another species. This small-scale prey
selection process (in the top 197 ft [60 m]) appears to be vital for the
survival of zooplankton communities as varied as those found in surface
waters.

Other examples of habitat compartmentalization are the distribution
of euphausiids swarms at different levels in the Benguela ecosystem, and
the selection by hyperid copepods of different species of gelatinous
zooplankton (situated at different depths) as substrates for
establishment and for feeding when environmental resources become
scarce. In zooplankton communities, interspecific relations are much
more subtle than was thought until recently. One case is the
compartmentalization of the habitat between the larvae of the anchovy
and the saurel in the North Atlantic. Anchovy larvae are less mobile and
their small mouths allow them to capture small prey, but they form large
swarms. The more active larvae of the saurel capture larger prey that is
less common but energetically more profitable.

3.4 Interspecific zooplankton relationships

Interspecific relationships at a small scale and an intermediate
scale are reflected in the structure of zooplankton trophic chains,
while in zooplankton communities biological processes are coupled to
physical processes on the same scale.

Trophic relations

Trophic relations are usually highly complex, as it is necessary to
consider not only the abundance of prey and predators, but also the
possibility of the two coming into contact in the planktonic
environment. This is exemplified by the trophic relations in the
communities of the coast of the island of Vancouver.

An example of the complexity of the trophic chains in the plankton
system is a community consisting of 1,000 individuals per 1.3 cubic yard
(1 [m.sup.3]) of the copepod Pseudocalanus minutus (1 mm in size), 400
of the copepod Calanus plumchrus (4 mm), and 10 of the euphausiid
Euphausia pacifica (20 mm), which are all competing to graze on a
population of diatoms of the genera Chaetoceros (23 microns). The
euphausiids consume most, reducing the population of Chaetoceros by 50%
and leaving the rest for the copepods. The copepod Calanus plumchrus
compensates its diet when it finds a swarm of a flagellate of about 10
microns, while Pseudocalamus minutus eat Chaetoceros.

After a few days, large quantities of euphausiid eggs are produced,
and in three or four weeks these will give rise to a new generation of
larvae that compete with the swarm of Calanus plumchrus to eat the
flagellates. The two species thus have a higher rate of production than
Pseudocalamus minutus. The development of swarms of larvae and of
Calamus plumchrus compared with that of P. minutus means that they are
detected more easily by the larvae of the salmon Oncorhyncus gorbuscha,
up to 8 mm long. Possible secondary predators of salmon larvae include
jellyfish (considered voracious predators of fish larvae) whenever
swarms of the two coincide. Jellyfish also compete successfully with
fish larvae, consuming larger quantities of copepods. At this stage
salmon larvae prefer copepods of smaller species (and their larval
phases), while the medusas take the larger species.

Recent studies in Chesapeake Bay have shown that in one day a
population of the scyphomedusa Chrysaora quinquecirrha can reduce the
copepod community by more than 90%.

Biological and physical processes

The development of a species from its origins until it reaches
sexual maturity follows a spatial and temporal development path that
depends on the structure and dynamics of the bodies of water it comes
across during its life. One example is the life cycle of the herring
(Clupea harengus) off the coasts of Scotland. The adults spawn in an
area of the continental platform where turbulent conditions favor the
eggs' buoyancy, enabling them to float. A current bears the eggs
north and the larvae find food easily when they hatch, as they are near
the densest plankton patches. As the larvae grow, they drift within the
same water mass that contains a rich zooplankton community. Calanoid
copepods growing at the same time give rise to several generations that
allow the larger larvae to find swarms of larger prey. The larvae have
already reached juvenile form and size when the current bearing them
deviates towards the coast, forcing them to migrate towards the bottom
and to swim actively back to their area of origin. During their
development, the water mass protects them from many predators without
isolating them from their food supply.

Deep-water zooplankton

In the high seas, life in the depths is a little different from the
description already given. That part of the ocean that is deeper than
0.62 mi (1 km) occupies almost 75% of the space where life is found on
Earth. This large space is totally lacking in light, even ultraviolet,
and on an oceanic scale varies little in temperature and salinity. The
organisms that develop in these quiet water masses are of relatively
little-known types because they are difficult to trap with traditional
sampling techniques.

Recent studies with submarines have made it possible to observe a
living system that is much more complex than previously thought.
Organisms are widely dispersed in the oceans and, except for some
crustaceans, displace themselves slowly. Gelatinous organisms--such as
siphonophores, medusas, salps, ctenophores, and pteropod mollusks (sea
butterflies)--are the most common. They are very large in comparison
with surface forms and have a life expectancy of several years. They
have delicate transparent bodies because they do not need to protect
themselves from ultraviolet light. They have neutral buoyancy and
although they are carnivores, they can pass long periods without eating.
Some are strong swimmers, capable of moving many kilometers a day.

The scarcity of resources has meant that gelatinous organisms
develop very sophisticated hunting techniques. For example, a colony of
physonectid siphonophores no more than 1.6 ft (0.5 m) in size extends a
complex net of fine tentacles that may reach 66 ft (20 m) in diameter.
Other species develop interspecific relations, such as hyperiid
amphipods, which live in association with medusas or even within their
gelatinous bodies. They exploit some of the prey captured by the medusa,
as well as eating the medusa itself if necessary. Many of these
gelatinous organisms form dense populations, especially the physonectid
siphonophores, which have gas in their pneumatophores, and their
distribution in the deep sea coincides with what is called the deep
scattering layer (DSL). The fact that they are so common has led to talk
of a predator zone in the middle layer of the water, spread throughout
all the oceans.

4. Secondary and tertiary consumers: large invertebrates and
vertebrates

4.1 A bountiful but dangerous environment

Lacking the refuge and cover provided by the substrate, the
organisms inhabiting the pelagic environment are surrounded by food, but
also run the risk of being eaten. As already pointed out, in addition to
the permanent plankton there are many eggs and larvae that are there
temporarily. It is not uncommon for the larval stage of some large
predators to be consumed by adults of species that form part of their
normal prey. Most organisms pass through different stages in which they
are primary consumers when they eat phytoplankton, secondary consumers
when they change to eating zooplankton, and finally tertiary or greater
consumers when they reach adulthood.

In general, pelagic organisms show greater diversity in tropical
regions than in temperate ones, which in turn show more diversity than
cold ones, However, especially on the continental platforms, the
specific diversity of pelagic organisms in each biogeographical region
is lower than that of their benthic equivalents. The diversification of
forms is closely related to the heterogeneity of the environment: the
larger the number of microhabitats in an environment, the larger the
number of forms that can develop in the ecosystem. The relative
homogeneity of the pelagic medium does not lend itself to
diversification.

The fact that few forms are possible means that natural selection
is undeniably more severe because it is not possible to avoid
interspecific competition through specialization. However, the abundance
of pelagic fish is notably greater than that of benthic species, given
that they are intimately related to the layer of most important primary
and secondary producers, and because the absence of high diversity
favors the concentration of biomass in a few species.

The main taxonomic groups represented at the level of secondary or
tertiary consumers in the pelagic environment are fishes, some
crustaceans (especially euphausiids and galatheids), some mollusks
(squid and cuttlefish), birds, and mammals.

Survival strategies

In a pelagic environment it is not possible to apply most of the
strategies that benthic organisms employ to improve their chances of
living and leaving offspring (adopting cryptic coloration, burying
themselves in sand, seeking shelter among rocks, covering themselves
with other organisms to blend in with the substrate, etc.). In the
pelagic medium, the only appreciable differences in a given point of the
water column are the light colors (above) and dark colors (below), with
variations due to reflections and waves. The only possible cryptic
coloration is the lack of color, or what is called countershading, which
consists of having a dark, shaded dorsal surface which will not stand
out against the ocean bottom when seen from above, and a clear,
reflective ventral surface that may be mistaken for the surface when
seen from below. This type of coloring also makes the organisms less
conspicuous because the dark dorsal color compensates for the
illumination it receives from above, and vice versa. Most organisms that
live in the euphotic zone of the pelagic environment have this sort of
coloring. Other defense strategies are based on the velocity of
displacement or in the grouping of many individuals into compact
patches. Despite this, predation is intense and most pelagic organisms
are eaten before they reach adult age. In these conditions of exposure
to predation, populations obviously require strategies that ensure
sufficient survivors for reproduction. Thus, currently, the only species
in pelagic ecosystems are those that have achieved this type of response
to intense selection.

These responses by the population include strategies based on rapid
growth and the production of many offspring, a tactic present to a
varying extent in small, medium, and some large species. Another
specific strategy consists of being large from the beginning and
protecting the young. Both sharks and cetaceans use this type of
survival strategy. Finally, the pelagic environment attracts organisms
that are temporary residents there and eat the permanent residents, and
then reproduce outside this very risky environment. This is the strategy
adopted by seabirds and pinnipeds.

Genuinely pelagic fish usually produce large quantities of eggs,
some as many as a million. The small fish grow and mature as quickly as
possible in order to reproduce before they are eaten; most small fish
have a lifespan of less than six years, and start to reproduce when they
are three. Strictly pelagic octopus and cuttlefish usually only live for
one year and most females die after reproducing. Other medium and large
fish tend to grow and reach the adult state rapidly, and so contribute
to reducing the level of predation by other species. Some tuna grow
until they are a thousand million times heavier than when they left the
egg! In general terms, the transference of energy to the pelagic
environment follows the ecological principle that adults increase their
adult size and reduce their biomass with increasing distance from the
primary producers of their trophic chains. This principle has many
exceptions in any environment, and some of the most notable are in the
pelagic ecosystem. The largest animals that have ever existed on the
planet shorten the food chain and basically eat zooplankton.

Migrations are also a common characteristic of the pelagic
environment, and most nektonic species migrate in one form or another.
Many organisms, especially those of oceanic tropical regions, show daily
vertical migrations. Mesopelagic fish are an example of vertical
migration of great importance. However, horizontal migrations are more
spectacular. The distances that can be covered by the larger organisms
of the pelagic environment are impressive: There are reports of
migrations of nearly 10,000 mi (18,000 km). Sometimes the precision of
migration is surprising, especially in organisms that reproduce in
exactly the same place as they hatch. Bearing in mind that this
environment is almost entirely lacking in visual references, this is an
astounding achievement.

Productivity in pelagic systems

As explained before, the distribution of productivity in the ocean
is not at all uniform, although superficially all seas look the same. In
general terms, the continental platforms are much richer than the open
sea, seas at high latitudes are richer than those in the tropics, and
upwellings are the most productive areas. The poorest areas of the
pelagic environment are, of course, the centers of the large gyres, one
in each hemisphere and in each ocean. The richest areas are those where
upwellings favor extraordinarily high productivity. Pelagic species are
most abundant in regions where productivity is very high.

The ecological efficiency (i.e., the proportion of energy
transferred from one trophic level to the next) also changes greatly.
Areas of upwelling are much less efficient than tropical areas, as their
production is so high that there are no effective mechanisms to use it
fully, and much sinks to the bottom.

The existence of many strata of diatom remains and phosphorite
deposits is clear proof of this considerable loss of production. The
situation is totally different in tropical oceanic ecosystems; their
primary productivity is much lower and their ecological efficiency is
much higher, and all the organic material is used at the top of the much
deeper water column. The production that occurs in the photic zone is
consumed, degraded, and remineralized in the top 1,640 ft (500 m). There
are almost no organic remains on the ocean bottom in the central regions
of the oceanic gyres. Even though the transfer coefficients between
levels are three times greater in poor ecosystems, the difference in
primary productivity between rich and poor ecosystems is usually very
large.

Production cycles

The abundance and reproduction of pelagic species depend not only
on the ocean region, but also on the annual cycles of the species they
eat. Production cycles show wide amplitudes (i.e., there is a large
difference between the average minimum and maximum productivity within a
year) in high latitude regions where periods of maximum productivity are
short. Pelagic organisms in these areas have very short reproductive
seasons, and in the case of the herring (Clupea harengus) it only lasts
two or three weeks. The synchronization of reproduction is thus crucial
in an environment where high production favoring larval food supply
lasts only a short time.

In temperate upwellings, high productivity lasts longer and
reproductive seasons may be much longer. Spawning by the California
sardine (Sardinops caerulea, S. sagax) may peak over a period of three
to four months. Furthermore, depending on the area where the population
spawns, there may be a single peak for the entire year (for example to
the south, off California), or two (for example in Magdalena Bay, in the
southwest of the Baja California peninsula). In cold years, spawning in
the first region may be limited to a few weeks, but in hot years it may
occur in almost every month of the year.

In tropical zones, spawning usually occurs throughout the year, as
reproductive cycles show minimum amplitude between different months. In
this case, spawning may be restricted to an area within the oceanic gyre
that is upstream from the area most suitable for larval growth, so they
will drift to areas where they have a greater chance of surviving.

Exploitability of the pelagic environment

In the middle of the 20th century when catches were growing faster
than world population, there was a generalized optimism that the ocean
might represent humanity's greatest food reserve. Serious
researchers calculated that total world catches could reach 200 million
tons before the year 2000. This goal now appears quite unattainable.
Potential catches have recently been recalculated, suggesting that an
annual catch of 140 million tons might be possible, if current catches
were adequately administered and as yet unused traditional resources
were also exploited.

Although it is clear that the potential of the pelagic environment
is much greater, the exploitation of these large volumes is not as
simple as it once seemed. Some species cannot be caught economically
using contemporary technology. Even if new technologies gave humanity
access to these non-traditional resources, we would be in a difficult
dilemma. Should we seek to increase catches by catching species at lower
trophic levels? The need for raw materials and food might require a
decision of this nature.

Most fish consumed today belong to higher trophic levels and
changing fishing objectives would have important repercussions because
humans would come into competition with these species for food. We may
well end up exchanging one kilogram of tuna for 10 kilograms of lantern
fish (Myctophidae). Maybe future imagination will find practical ways of
solving the oceanic paradox of a nutrient-poor illuminated photic layer
resting on a nutrient-rich layer lacking light.

4.2 Typical pelagic consumers

Trophic chains in the pelagic environment are generally short.
Furthermore, apart from a few exceptional cases, they are poorly
defined. The smallest fish, for example, are primary and secondary
consumers, as they eat phytoplankton and zooplankton. The smaller
secondary (mid-sized pelagic) consumers basically eat zooplankton,
although they also consume juvenile fish. The larger members of this
group are definitively ichthyophagous (fish-eating) and eat the smaller
pelagic species.

Squid and cuttlefish exemplify the poor definition of trophic
chains in pelagic environments. They consume fish and large plankton,
and in turn they are food for a wide range of higher-level consumers.
One particularly interesting trophic chain occurs in tropical areas
where mesopelagic fish (especially Myctophidae) eat zooplankton and are
eaten by tuna. Most researchers refer to production of
zooplankton-eating fish and their consumers as tertiary production;
although this is not strictly true, it is a practical and convenient
approach.

Fish and small crustaceans

The larvae of many species of pelagic and benthic fish live in the
plankton during a short but important part of their life. Their enormous
abundance means they play a large role in the energy flow of the
ecosystems.

Apart from these organisms, normally studied as part of the
zooplankton, only a few types of adult small-sized fish are found in
abundance in the pelagic environment: some Clupeiformes (herring,
sardine, and anchovies); the mesopelagic species, mostly Myctophiformes
(lantern fish); and skippers and related species (Scomberosocidae). Of
course, there are many other species of fish in the pelagic ecosystem,
but they are much less abundant and much less important within the
community's energy flow.

Together with some crustaceans and other organisms of the
micronecton, small fish represent the most important link between
primary production and secondary production within the rest of the
trophic chain in the pelagic environment. They are very abundant
compared with the other species and form the basic prey of larger fish,
in both the pelagic and in much of the benthic environment. This is
partly explained by the fact that these small fish (especially
Clupeiformes) may obtain part of their food from the phytoplankton given
that their symbiotic intestinal bacteria can produce cellulase. The
resulting shortening of the trophic chain means that these populations
can reach a very high biomass.

Sardines and anchovies

Although more than 300 species of Clupeidae belonging to 80 genera
are recognized in the specialist literature, the two main genera
Sardinops and Engraulis (sardines and anchovies) represent more than 60%
of the total world catch of Clupeiformes, which in turn constitute about
20% of the total world sea and freshwater fish catch. Both genera
include various species or populations of sardines and anchovies of
warmish waters where temperate and tropical waters mix. Most of these
areas are found where upwelling occurs, on the eastern barriers of the
great oceanic gyres, off California, Peru-Chile, the Canary Islands, and
Benguela. However, one of the most important regions where these
Clupeidae live is around Japan, where there is no upwelling. In each of
these areas of special abundance, the populations of these two genera
represent the dominant small fish of the system. Other genera of
Clupeidae, such as Sardina or Sprattus, occupy the same position as
Sardinops in the Canary Current and in the Mediterranean, where they are
also very abundant.

One of the most surprising characteristics of these fish is that
their abundance varies drastically over very short periods of time. The
best-known and most impressive example is the Peruvian anchoveta
(Engraulis ringens), catches of which fell from nearly 13 million tons a
year to almost nothing in less than a decade. The populations of
sardines (Sardinops) in Japan and in Peru and Chile, on the other hand,
grew so much that the combined catches reached more than 10 million tons
in less than ten years. The relative abundance of one or the other genus
has been checked using historical records, and when sardines were
abundant, anchovies were scarce, and vice versa. Even so, it is more
interesting to know that these alternations occur in parallel in areas
sometimes separated by whole oceans. The coherence of the synchronic
behavior of sardines and anchovies in Japan, Chile and Peru, and
California, and in their simultaneous changes (although they are out of
phase, as the anchovy is abundant when sardines are abundant in the rest
of the systems and vice versa) in the Benguela Current seems to
demonstrate that there is some cyclic factor of a planetary nature that
determines the dominance of one population or the other.

Some upwellings have almost anoxic areas of sea floor that preserve
organic remains especially well. Analysis of these areas has shown that
the scales of many fish are preserved perfectly in strata of deposits,
called laminated sediments. This type of deposit has been analyzed off
Baja California, both in the ocean and in the Gulf of California, and
also in South Africa. Samples are also now being studied in other
regions. Although it used to be thought that fishing was the factor
determining the relative abundance of the populations of anchovies and
sardines, analysis of scales found in laminated deposits of several
systems has shown that these populations typically showed large
fluctuations in abundance long before they were exploited by human
beings. Independently of the fact that fishing magnifies and accelerates
changes in abundance, they occurred in the past and will surely continue
to occur in the future, as a reflection of the profound changes, as yet
little-known, that affect an entire ecosystem.

Herrings

Herrings (Clupea harengus) are particularly abundant in the
north-eastern Atlantic, where they are one of the most traditional
catches. They reproduce close to the substrate and deposit their eggs on
the seafloor near the coast. When the eggs hatch, the larvae form part
of the plankton. Spawning is closely linked to environmental conditions:
The date of spawning can be calculated for each population to within
roughly a week. Furthermore, it has been shown that about 80% return to
spawn in the same place where they hatched, and the remaining 20% allow
recombination between populations. There are also herrings in the
northern Pacific, although they are considerably less abundant than in
the Atlantic. In terms of biomass, herrings are the most important
clupeids that make use of periods and areas of high productivity in the
cold-temperate seas.

Other clupeids

Other clupeids are coastal and channel primary and secondary
production from the continental platform, the most productive areas.
There are also Clupeidae in more tropical regions although their biomass
is much less than those of temperate and cold-temperate waters, which
produce about 80% of all the catch of clupeids. The most abundant genera
include Brevoortia, (the "menhaden" of the coasts of the Gulf
of Mexico and the southeast of the United States), Sardinella (the
anchovies of the Atlantic, Indian and Pacific), and Opisthonema (of the
tropical coasts of the American Pacific).

Small mesopelagic fish

In regions further from the coast, the main fish are oceanic
mesopelagic species that live in the intermediate layer of the deep
seas. They normally live at depths of between 656 and 3,281 ft (200 and
1,000 m) in the photic (epipelagic) layer, between the level where 1% of
the incident light penetrates and the greatest depth light reaches. They
are usually distributed beyond the slopes around every continent and
island. These areas account for about 22.5% of the total surface area of
our planet's oceans.

Many species perform daily vertical migrations, rising to the
surface in the afternoon to eat in the zooplankton-rich waters. Some
even arrive in the surface layer during the night. When the sun comes
out, they descend back to their usual depths. They are so abundant that
they form most of the deep scattering layer, an echo that appears in
deep soundings and moves vertically between sunrise and sunset. Their
eggs and larvae form part of the meroplankton and are the highest
biomass of any type of vertebrate in the oceanic plankton. They form an
unexploited reserve of millions of tons.

This group of fish, the largest portion of the biomass of the
mesopelagic zone, is made up of about 700 species in the entire world.
Their relatively large eyes allow them to see in the twilight conditions
of the mesopelagic layer, and many have tubular eyes to concentrate
light. Their jaws can open very widely, and catch prey and eat pieces of
dead animals or even entire corpses of their own size. They possess
numerous photophores on the ventral surface, said to confuse predators
that hunt them from below against the scarce light that penetrates from
the surface of the sea.

There have been limited efforts to catch these fish, especially in
South Africa. Most are processed for fishmeal and oils, but they contain
so much oil that these products are difficult to extract using
conventional procedures, because they clog the machinery. The direct
consumption of some of the larger species has had an unenthusiastic
reception, mainly because some have high concentration of waxes and
esters in their flesh. Their exploitation is difficult because of their
small size (most species are between 2-4 in [5-10 cm]) and the fact they
are very dispersed (one individual per 1,308 cubic yards [1,000 cubic
meters]), quite unlike the clupeids, which form very compact masses that
are profitable to exploit.

Mesopelagic fish basically eat zooplankton and in turn form the
main food of many larger species, such as tuna, mackerel, squid,
pinnipeds, and cetaceans, especially some rorqual whales and many
dolphins.

Mesopelagic fish form part of the trophic chain, actively
transporting energy towards the bottom. As opposed to the passive
sinking of corpses and waste products, mostly consumed in the layer
where they originate or in the layer immediately below, this form of
transference is based on the daily migration of organisms from deeper
layers to the surface to feed. Here they are, in turn, food for
organisms of the underlying layer, and those of lower layers, and so on.
The original conception of a photic zone producing surplus biomass that
slowly sinks and is consumed by different organisms is difficult to
reconcile with the dynamic recycling of nutrients within each level of
the long water column of the deep oceans.

The Scomberesocidae, such as the skipper (Scomberesox saurus) and
other similar species, are pelagic fish 8-14 in (20-35 cm) long when
adult. Their abundance makes them an important link in the trophic chain
and they connect the zooplankton's secondary production to larger
fish, especially tuna, and many birds. Although they do not reach the
volumes of the two groups discussed above, their importance lies in the
fact that they live close to the surface and far from the coast. There
are scomberesocids in the Pacific and the Atlantic.

On the Pacific coast of the United States calculations suggest a
biomass of almost 500,000 tons. Japan has been one of the main countries
fishing these species and recently catches have reached 250,000 tons.
The scombereosocids belong to the order Beloniformes that also includes
other pelagic species, such as halfbeaks (Hemirhamphidae) and flying
fish (Exocoetidae), relatively important in coastal tropical waters.

In the Antarctic Ocean there are two species of small fish that
occupy an equivalent trophic level: Pleurogramma antarcticum and
Notolepis coatsi. Both are relatively abundant, consume zooplankton and
are eaten by larger animals. The first is eaten by penguins and seals,
and the second by rorquals.

Pelagic microcrustaceans

Some pelagic microcrustaceans exist at this trophic level of
phytoplankton and zooplankton consumers. Euphausia superba, Antarctic
krill, is usually considered as a component of the zooplankton and is
not discussed here. However, some galatheids such as the Chilean
crayfish (Munida gregaria) of Chile and New Zealand, or the Mexican
shrimp (Pleu-roncodes planipes), are very abundant and of great
importance in the trophic chain in some areas.

During the first years of their lives, these small reddish crabs,
(which in Chile are called langostinos, or crayfish) have a pelagic
phase and later become benthic. During their pelagic phase they form
extraordinarily abundant concentrations and, on occasions, they even get
beached in large quantities. They eat both zooplankton and
phytoplankton, and so are similar to the clupeids, inasmuch as they do
not channel productivity towards higher trophic levels. The Chilean
crayfish has been caught commercially in Chile, processed to obtain the
relatively small tails, and then exported at a good price.

Mexican shrimp are a favorite food of the tuna during the part of
their annual migration when they penetrate the California Current, when
they may even form 85% of the tuna's food. They are also among the
few organisms grey whales (Eschrichtius robustus) eat during their stay
in the warm-temperate waters in the coastal areas of the Baja California
where their young are born during the winter season.

Medium-sized fish

Medium-sized fish form the least defined category of the entire
trophic chain found in the pelagic environment. Some are only slightly
larger than small fish and their food includes zooplankton,
microplankton, and the juvenile stages of other fish and squid. The most
abundant genera of medium-sized fish belong to the scombrid family
(Scombridae), the mackerel (Scomber) and the Spanish mackerel
(Scomberomorus), or to the carangid family (Carangidae), such as the
saurel (Trachurus) and jacks or kingfish (Seriola).

Some important genera that do not belong to these two families are
Mallotus of the osmerid family (Salmonidae) and Micromesistius,
including the blue whiting (M. poutassou), a member of the gadid family
(Gadidae). Micromesistius, exceptionally for a member of the normally
benthic gadiforms (Gadiformes), is mainly pelagic but tends to form
extensive layers rather than dense masses. The capelin (Mallotus
villosus) is a mainly arctic gadid found to the north of the polar
front, off the coasts of Canada and Norway, and in the Barents Sea. It
is fished in the north and the southeast of the Atlantic. The catch of
each of these genera has exceeded 100,000 tons a year, a figure that
demonstrates their abundance. Many other genera of these two families
are also present in the pelagic environment, especially on the
continental platforms of tropical seas.

Another important family in this category is the Sphyraenidae,
represented by the barracudas (Sphyraena), medium-sized predators that
basically eat small fish and squid.

Bathypelagic fish

The bathypelagic (between 1,640 ft [500 m], the lowest level with
light reaches, and 9,842 ft [3,000 m]) and abyssal (down to 6 mi [10
km]) subdivisions form most of the pelagic environment. The ecosystem of
these deep seas is almost totally heterotrophic, dominated by
catabolism, and allochthonous, in the sense that the energy necessary
for its existence has to come from somewhere else.

In addition to the absence of light, most of the water is cold and
the seasonal variations in temperature are almost imperceptible. The
physical and chemical characteristics of the water correspond to the
high latitudes where they formed. Water from the circumpolar areas takes
a long time to flow along the seafloor to the equator. The deep water of
the Atlantic, for example, is probably 200 to 300 years old, while that
of the Pacific is definitely 1,000 years old. Variations in the
environment of the deep ocean make sense only on a geological
time-scale.

Just as upwellings on the surface are very important because they
bring nutrient-rich water up to the photic zone, turbidity currents
appear to be the most relevant phenomena in the deep sea. Immense
cascades carry sediments down to the poor seafloor, bearing organic
remains and covering part of the deep fauna.

It has been shown that the abundance of organisms diminishes with
depth in a way that is exponential (but not regular). There is a clear
tendency for organisms to be less dense as depth increases, probably to
increase metabolic efficiency and conserve energy, as it reduces their
need to maintain themselves floating at a specific level. The deeper the
fish lives, the greater its water content in comparison with proteins,
carbohydrates, lipids, and skeleton.

Bathypelagic fish show the most profound modifications found in
fish living at any depth. They have large jaws and teeth, and many
possess barbels to attract prey. Deep-sea devils (Ceratiidae), for
example, have a photophore-bearing "lure" appendage above
their usually very small eyes. Many females seem to emit pheromones to
attract males that have a highly developed sense of smell. This helps
the different sexes to find each other in a world without light. Sexual
dimorphism is common and can be extreme; the males of Ceratias are much
smaller than the females, and when they locate a female they attach
themselves and gradually degenerate until they are little more than a
small sac with reproductive organs. Bathypelagic fish undergo even more
profound changes than the benthopelagic fish, which are much more
related to the seafloor. These fish, such as the ghostfish
(Chimaeridae), the ratfish, and other Macrouridae and some rays look
much more familiar.

Squid and cuttlefish

Cephalopods, especially the squids (Loligo, Todarodes, Abralia,
Illex, etc.) and the cuttlefish (Sepia) are a very important component
of pelagic ecosystems, although only a minimal part of their population
is exploited by human beings. Nearly all the squid catch comes from
waters less than 656 ft (200 m) deep, a very small part of the oceans.
Larger squid live at greater depths.

The abundance of larger species of squid (Architeuthis), has been
estimated partially on the analysis of remains (especially of the
mandibles) found in the stomachs of sperm whales. It has been calculated
that these large mammals alone consume 100 million tons of squid a year,
in other words, more than the total caught by humans throughout the
world. In the Antarctic, where predation of squid by cetaceans has been
studied, it has been calculated that squid consumption by sperm whales
represents about 35% of the total consumed by all predators.

Pelagic squid mainly eat small fish although they may also consume
some crustaceans, including copepods and galatheids, as well as pteropod
mollusks and other squids. Squids' food conversion (ecological
efficiency) is among the highest known: About 50% of the fresh weight
consumed is incorporated into the organism.

Large fish

The subclass Scombridae includes medium- and large-sized fish,
active predators at high trophic levels. These include tuna (Thunnus),
bonito (Sarda), Luvarus, mackerel (Scomber), the cutlassfish
(Trichiurus), marlins or spearfish (Tetrapterus), and swordfish
(Xiphias). All of them are adapted to permanent movement and speed; the
sailfish (Istiophorus platypterus) has been timed at more than 68 mi/h
(110 km/h). They are the most hydrodynamic of all fish; their fins fold
into a special groove, and their eyes form a smooth surface flush with
the rest of the head. They cannot stop swimming for two reasons. The
first is that they depend on the oxygen transported in the water flowing
permanently through their open mouth, as they have lost most of the
mechanisms used by other fish to pump water through their gills. The
second reason is that if they do not swim, they sink, because they are
denser than water, partly because they lack a swim bladder.

This permanent movement requires a considerable expenditure of
energy; some species consume up to 25% of their body weight every day.
Their intense metabolism generates a large quantity of heat, meaning
that they, and tuna in particular, are warm-blooded animals. They
possess unique physiological mechanisms to dissipate the excess heat,
including an intricate network of fine blood vessels called the rete
mirabilis. As efficient predators they have very sensitive hearing,
sensitive chemical detectors, and a stereoscopic vision so they can
measure distances. They are also very prolific; the females release
100,000 eggs per kilo of body weight; so a 110 lb (50 kg) female
produces about 5,000,000 small eggs. Starting from an egg just one
millimeter in diameter, the tuna (Thunnus thynnus) increases a thousand
million times in weight to reach its adult weight of more than 1,542 lb
(700 kg). The black marlin (Makaira ampla) may reach more than 2,863 lb
(1,300 kg); it is without doubt the largest bony fish in the seas. They
are remarkably migratory; the albacore (Thunnus alalunga) migrates from
the coast of California to Japan, about 5,282 mi (8,500 km), and even
greater distances have been recorded for other species of the same
group.

Other large fish include the dolphinfish or "mahi-mahi"
(Coryphaena) and the sea cock (Nematistius), well-known but
comparatively scarce. One particularly important group in the pelagic
environment, especially in the open ocean, is the sharks; without a
doubt they are among the most important predators of the entire ocean.

4.3 Allochthonous pelagic consumers

Fish and crustaceans are truly marine animals. Marine food chains
also include typically continental animals, such as carnivorous birds,
reptiles, and mammals specialized in exploiting fish stocks. These
groups show a wide range of strategies--ranging from coastal fishing
(seagulls) to capturing prey on the high seas (petrels), and from life
on the land with incursions into the sea (sea otters) to permanent
adaptation to marine conditions (cetaceans).

Marine turtles

Marine turtles belong to two different families: the Dermochelidae
(leatherbacks), with one genus (Dermochelys), and the Cheloniidae, with
four genera (Chelonia, Caretta, Lepidochelys, Eretmochelys). The
leatherback turtle (Dermochelys coriacea), one of the largest reptiles
in existence, belongs to the Dermochelidae. The adults are easily
recognized by their coriaceous (leathery), scaleless carapaces (shells).
This species has the widest distribution of the marine turtles and lives
in colder water than the others. In autumn and winter they move in very
large groups. The main beaches where they nest are on the western coast
of Mexico (80,000 nests a year), in Guyana (10,000-15,000), in Costa
Rica (5,000), and in Trinidad and Tobago (1,000). The coasts of Malaysia
also used to be important, but the number of nesting areas has now
fallen greatly. On other tropical coasts the number of nests is much
lower. The other family, the Cheloniidae, includes important species,
like the loggerhead turtle (Caretta caretta), green turtle (Chelonia
mydas), Pacific ridley (Lepidochelys olivacea), Kemp's ridley (L.
kempi), flatback turtle (Chelonia depressa), and the famous hawksbill
turtle (Eretmochelys imbricata), which used to be exploited for its
carapace. It is the most tropical of the marine turtles and is
distributed in the coastal Atlantic and the Indo-Pacific, and breeds in
the spring and summer.

Marine mammals

Marine mammals include the largest consumers found on the entire
planet, not just the oceans, and the largest organisms known to have
existed. The large majority of marine mammals are found in the
circumpolar regions, or the temperate areas of high productivity caused
by upwelling or the mixing of waters. In any case, it is obvious that
these organisms have developed in a special way in those areas where
there is a wealth of food available. One group of mammals, the pinnipeds
(walruses and sealions), uses the pelagic environment in the same way as
birds; they eat there, but escape its more dangerous aspects by
reproducing on land.

Not all marine mammals eat mainly pelagic organisms. On the
contrary, many of them preferentially consume species from the seafloor.
This is the case in some seals (for example Erignathus), walruses
(Odobenus), some dolphins, the narwhal (Monodon), and even a whale, the
grey whale (Eschrichtius). In general terms, because of the large area
of continental platform in this region, many of the marine mammals in
the Arctic eat organisms from the ocean bottom. In the Antarctic, most
species depend almost entirely on the pelagic environment for their food
supply, as there is almost no shallow seafloor. (see volume 9).

Dolphins are active consumers of pelagic organisms, especially
small fish and squid. There are many species of dolphin distributed
throughout almost all the oceans, although they are considerably more
abundant in zones of high productivity. The largest organisms of all,
the whales (of the family Balaenidae), have shortened the food chain by
eating basically zooplankton and, in some cases, small pelagic
organisms.

The Antarctic Ocean and the Arctic Sea are their most important
feeding areas during the summer. The Antarctic, to be precise, has four
times more whales than the entire northern hemisphere. Its main
attraction is the enormous abundance of zooplankton and micronekton,
which grows extraordinarily quickly and forms enormous, dense patches.

The whales that feed in the pelagic environment have two methods of
feeding. The first is characteristic of the whales with flippers (family
Balaenopteridae), and consists of gulping a huge quantity of water (up
to 78.5 cubic yards [60 cubic meters]), and filtering it through the
baleen plates that retain the zooplankton. The other is characteristic
of the right and bowhead whales (family Balaenidae), and consists of
swimming close to the surface with their mouths open and baleens closed,
like a net. Both methods require abundant prey to compensate for their
energetic cost and to leave enough surplus for normal metabolic
expenditure and for growth and blubber accumulation.

Seabirds

Seabirds are very important predators of the pelagic environment.
In some places, guano deposited by seabirds on coastal islands has been
used as a fertilizer and used to be collected in large quantities,
especially near upwellings like the Humboldt Current and the Benguela
Current.

Many species of bird--such as gulls, cormorants, pelicans and
penguins--feed basically in the pelagic environment. Although many eat
benthic organisms such as crabs and mollusks, in terms of food volume
there is no doubt that small pelagic animals are their main food source.
In fact, one major effect of the "El Nino" (heating of the
Pacific of equatorial origin) is the widespread mortality of marine
birds, as the schools of Peruvian anchoveta, their main prey, move to
lower depths than normal and are not accessible to the birds.

The degree of adaptation to the pelagic environment is reflected in
the feeding methods of each group of birds. The range of variation is
very wide. There are species that belong to clearly terrestrial
taxonomic groups, for example, the osprey (Pandion haliaetus), is a bird
of prey that obtains its prey flying low over the surface of the water.
There are other species, such as frigatebirds (Fregata), fully
identified with marine environments, which do not submerge or swim and
obtain their prey by seizing it from other birds that capture it
directly. Gulls (Larus) and pelicans (Pelicanus) obtain their food while
swimming on the surface or penetrating a short distance into the water;
only those species that usually swim close to the surface are within
their reach. Gulls not only consume fish but also considerable
quantities of benthic organisms. Cormorants (Phalacroco-rax) and gannets
(Sula) show greater adaptation and can dive to great depths to hunt
their prey. Even so, there is no doubt that pelicans (Pelecanus) show
the greatest adaptation to marine diving.

The world distribution of guano deposits shows that upwellings
support the largest biomass of birds that eat fish and nest on land.
However, it is in the Antarctic, where there are many penguins, that
seabirds' participation in the trophic chains of the pelagic
environment is most obvious (and this is why they are treated in volume
9).

The biomass of the seven species of penguins that live in the
Antarctic has been calculated to be about 500,000 tons, while the other
seabirds are only about 50,000 tons. The penguins' consumption of
small fish, krill, and squid has been calculated to be about 30 million
tons a year, more than a third of the total world fisheries' catch.

23 The marine environment is the largest of all the Earth's
environments. Although it cannot be inhabited by people, its food
resources have been known and used since antiquity. This Roman mosaic at
the National Archeological Museum in Naples, Italy, clearly shows the
range of seafood on Roman tables 2,000 years ago.

[Photo: Museo Archeologico Nazionale di Napoli / Scala]

24 The relationship be-tween the size and speed of planktonic
organisms, depending on the viscosity of the water. The speed attained,
multiplied by a linear dimension characteristic of each species, and
divided by the index of viscosity of the water, is equivalent to the
Reynolds number, a parameter that allows comparison of different
hydrodynamic behavior by individuals depending on the water regime
(laminar, turbulent, etc.). The triangles correspond to specific cases.

[Drawing: Jordi Corbera, bas-ed on Margalef, 1982]

25 Plankton nets have been essential for obtaining samples since
the first studies of marine plankton. The pictures shows two being cast
from an oceanographic vessel.

[Photo: Joan Biosca]

26 The Sargasso Sea lies at the center of the Atlantic Ocean
between the Azores and the Bahamas, and is surrounded by currents
isolating it from the rest of the ocean. It is one of the world's
bluest and most transparent seas, the result of its low nutrient levels.
Virtually the only external nutrients it receives come from the eddies
that split off from the meanders of the Gulf Stream. The false-color
satellite images use a color scale from red to violet to indicate
decreasing presence of chlorophyll and nutrients. The dark patches to
the east are areas where the satellite sensor did not capture images,
due to clouds or other reasons.

27 Sargasso (Sargassum) floating in the Bermuda Sea. Unlike other
phaeophytes and most macroalgae, sargasso does not live anchored on a
substrate but instead floats freely on the high sea. Its many air
bladders give it the buoyancy that makes this ecological strategy
possible.

[Photo: Peter Parks / Oxford Scientific Films / Firo Foto]

28 Secchi's disc, perhaps the simplest and most classic of all
the devices used in oceanography. It was introduced in the middle of the
19th century by the Jesuit astronomer Angelo Secchi (1818-1878),
director of the Pontifical Observatory. It is used to measure the
transparency of the water and consists of a weighted white disk 12 in
(30 cm) in diameter hung horizontally at the end of a rope. At the depth
where the Secchi disc can no longer be seen, the photosynthetically
active radiation is about 18% of that found at the surface, and at a
depth 2.7 times greater, this has decreased to, at most, 1%. The
consistent sensitivity of the human eye is surprising, as estimations by
different observers of the disappearance of Secchi disks in the same
water coincide nearly exactly. This is almost independent of the
diameter of the disk, as long as the disk occupies a large enough angle
of vision at depths close to disappearance.

[Photo: Jordi Camp]

29 A bloom of the cyano-bacteria Trichodesmium erythraeum off
Ribloon Reef, on the Great Barrier Reef, Australia. This is the only
genus of cyanobacteria that forms blooms like this, which are much more
common in other groups of phytoplankton.

[Photo: D. Parer & E. Parer-Cook / Auscape International]

30 Dinophytes, like other marine protoctists, have always
fascinated microscopists. Since the first drawing by the Danish
microscopist Otto F. Muller, many scientist have become artists in their
attempts to represent their many forms and varied behavior. These
drawings dating from 1915-1917 are the work of the American zoologists
Charles A. Kofoid and Olive Swezy, and the artist Anna L. Hamilton.
These two plates are from their large monograph The free-living
unarmored Dinoflagellata. The dinophytes represented are: Cochlodinium
miniatum (107), C. volutum (108), Gyrodinium herbaceum (109),
Gymnodinium submarinum (110), Amphidinium dentatum (111), Gyrodinium
virgatum (112), Cochlodinium scintillans (113), Pavillardia
tentaculifera (114), Cochlodinium convolutum (115), Gyrodinium
rubricaudatum (116), G. corallinum (117), Erythropsis hispida (127), E.
scarlatina (128), E. cornuta (129), E. extrudens (130), E. minor (131),
E. labrum (132), E. pavillardii (133) and E. richardii (134). Note the
range of colors and forms shown by the chromatophores (mostly pigments
with no photosynthetic role), the light-sensitive eyes of the genus
Erythropsis, and the extensible tentacles of the species of this genus
and of Pavallardia tentaculifera.

[Photo: Jordi Vidal]

31 Not all dinophytes are photosynthetic organisms contributing to
the primary productions of the water they live in. Many freshwater and
marine species show heterotrophic lifestyles, which are more complex and
varied in the sea environment. Some, such as Protoperidinium conicum,
can extend and withdraw a veil-like pseudopodium (pallium) that envelops
other cells, usually diatoms, which then undergo extracellular
digestion. Others, such as Paulsenella chaetoceratis issue pseudopodia
that penetrate and suck the cytoplasm of their prey, digesting it
intracellularly (mizocytosis). Although it is a freshwater species,
Gymnodinium aeruginosum does the same, but it uses its pseudopia to
acquire its prey's chloroplasts which its keeps alive and
functional, while digesting the rest of the prey's cytoplasm. The
case of Peridinium balticum is quite different, as it houses a small
intracellular symbiont that provides the food it could not otherwise
synthesize. There are also dinophytes that limit themselves to
phagocytosis of other organisms, and some that are intracellular
parasites and eat the cytoplasm surrounding them.

[Drawing: Jordi Corbera, from several sources]

32 Dinophytes are among the most common organisms in the
phytoplankton. Ceratium is one of the most diversified genera, with both
freshwater and marine species. The image to the left shows Ceratium
ranipes, one of the most spectacular warm-water species, because of its
two branched appendages. Noctilucas (Noctiluca), on the right, are
larger than dinophytes, reaching 0.08 in (2 mm) in diameter, and their
size and bioluminescence make them visible to the naked eye.

[Photo: Claude Carre]

33 Drawings of some cryptophytes. They are all small, especially
Plagioselmis prolonga, and vary greatly in color because of the range of
pigments they may possess. The pairs of drawings represent the same cell
from different angles.

[Drawing: Jordi Corbera, from data by Hill]

34 Chrysochromulina is a genus of prymnesiophyte known as
"killer algae," although it is not known how they cause the
fish mortality they are blamed for. In May and June 1988 a sudden bloom
of C. polypepis affected a large area of the Denmark Strait and the
Oresund and the southern coast of Norway, causing great alarm and some
fish mortality. This was due to obstruction of the fish's gills and
local oxygen depletion in some bays by the decomposition of masses of
beached algae and mucilage, rather than by any identifiable toxin. The
drawing on the left shows a different species of Chrysochromulina that
is slightly larger than C. polylepis, a species that occasionally
produces similar patches in the Mediter-ranean.

[Drawing: Ramon Margalef and Editronica]

35 The unusual appearance of many diatom frustules, with their
regularly-arranged clefts and pores, has made them a favorite for
research by microscopists. Many people have made collections of
preparations of diatom frustules, and they have been used as tests of
the quality of optical microscopes, or as a sort of microscopic
yardstick. The images show the complete frustule of a species of
Thalassiosira in connective view (top), an external valve view of T.
eccentrica (middle), and an internal valve view of an organism of the
genus Asteromphalus (bottom).

[Photo: Maximino Delgado and Jose Manuel Fortuno]

36 Some diatoms live in association with ciliates. This allows them
to remain in suspension without settling and also guarantees regular
renewal of the surrounding water, thus increasing their assimilation. It
is not clear what benefit the ciliate obtains from the association, but
it may obtain a more regular supply of bacteria--those growing on the
diatom or its appendages. Alternatively, the size and shape of the
association may prevent the ciliate from being eaten by zooplankton
predators. The photo shows an example of the association between
Tintinnus inquilinus and the diatom Chaetoceros tetrastichon.

[Photo: Claude Carre]

37 Some silicoflagellates can only live within a limited
temperature range. There is a close correspondence between water
temperature and the distribution of the two major groups of
silicoflagellates (those with four sides, included in the genus
Dictyocha, and the six-sided ones, in the genus Diste-phanus).
Distephanus types are generally found in waters below 59[degrees]F
(15[degrees]C), while those of Dictyocha cannot live below 50[degrees]F
(10[degrees]C). The transition between the two forms may be sudden, as
in the Sea of Japan, or they may coexist in areas with water
temperatures within their respective limits, as happens in the
south-western Atlantic.

[Drawing: Jordi Corbera, bas-ed on data from Lipps]

38 Biogeographic types of phytoplankton and their areas of
distribution. The geographical distribution of phytoplankton species is
still not well enough known to make generalizations other than a
provisional simplification that allows a convenient ordering of the
available data. That given here is based on a division of the oceans
into five great domains: cold northern waters, temperate northern
waters, warm waters, temperate southern waters, and cold southern
waters. These domains allow division into twelve biogeographical areas
to include all known species of marine phytoplankton. The approximate
percentage of each type is shown.

[Drawing: Editronica, based on data provided by the author]

39 Plankton diversity in the Mediterranean and the Caribbean is
among the highest in the world, and is probably only exceeded by some
points of the Pacific Ocean. These graphs show two comparisons between
plankton samples from the two areas, one in the north-west Mediterranean
and the other in the southeast Caribbean (1963 and 1965). The upper
graph shows the distribution of the two sets of samples grouped by cell
volume. In the Caribbean, smaller cells predominate and there are
relatively fewer larger ones. The lower graph arranges phytoplankton
species in decreasing order of total numbers of individuals. Only the
200 most abundant species in each set were included. Abundance is
expressed on a logarithmic scale (left). The values found are very
similar in both cases, with the Mediterranean showing a slight
advantage.

[Drawing: Editronica, based on data provided by the author]

40 Factors affecting plankton distribution. The left-hand diagram
shows the relationship between fluctuations in environmental conditions
and the presence of toxic dinoflagellates (Gymnodinium catenatum and
Protogonyaulax affinis) in the Vigo estuary (Spain) in autumn, 1985. The
water in a relatively resting state (low index of upwelling) coincides
with a high surface temperature and the development of toxic
dinoflagellates. The appearance of the coastal upwelling introduces cold
water and brings the "sea purge" to an end. The right-hand
diagrams shows the relationship among chlorophyll, nutrients, and light.
The observations made in the English Channel in July 1976 show the
tendency to reach, sooner or later, nutrient depletion where there is a
lot of light. The lower diagrams show more detailed sections of the
Baltic Sea, where chlorophyll peaks cluster around the maximum
temperature gradient.

[Drawing: Jordi Corbera, based on S. Fraga, Derenbach, and Pingree]

41 14C levels in the dissolved organic carbon oxidisable by
ultraviolet radiation in samples from the north of the central Pacific
(31[degrees]N, 159[degrees]W) and from the Sargasso Sea in the Atlantic
(31[degrees]50'N, 63[degrees]30'W). The 14C values are
indicative of the age of the dissolved organic carbon, given that the
concentration (in parts per thousand) diminishes with depth. As the
graph clearly shows, the deeper the samples are taken, the older the
organic material is. From this we can conclude that in the deep waters
of the Pacific there is more dissolved organic matter than in the
Atlantic, which confirms the Atlantic's relative youth. Note that
at 3,281 ft (1,000 m) there is a change in the vertical scale.

[Drawing: Editronica, from several sources]

42 Rapid phytoplankton blooms occur for no apparent reason in
different points of the ocean, such as this bloom of the cyanobacterial
genus Oscillatoria in the Pacific, off the eastern coast of Australia.
They are only possible because there is always a reserve of biodiversity
in the plankton, including a wide range of organisms in a more or less
quiescent state, but ready to make use of improved growing conditions.

[Photo: L. Newman & A. Flowers / Auscape International]

43 The concentration of phosphorus in seawater decisively affects
its fertility. Although on a global scale the phosphorus content of the
oceans is considerable (an average of 2.3-2.5 micromoles phosphorus per
liter), its concentration in surface water is negligible, as almost all
that arrives is immediately used by organisms. Only in certain upwelling
areas does a little phosphorus from deep waters and nutrient-rich
sediments enrich the surface, and even in these areas it is mainly
concentrated in deep water. This is shown by superimposing the values
for available phosphorus on those for chlorophyll on this section along
the parallel 26[degrees]S near Luderitz, Namibia, in the upwelling off
southwestern Africa during the southern summer. As in other upwellings,
the amount of unconsumed and non-dispersed production determines the
accumulation of organic matter and phosphorites in the sediments below,
as shown in the maps. The graph, corresponding to samples taken from
Septem-ber 19-21, 1985, also shows the areas dominated by different
species or genera of diatoms with different behavior with respect to
nutrients. Thalassiosira multiplies rapidly (chlorophyll peaks) and is
eaten by copepods. At the other extreme, the similar Planktoniella,
multiplies more slowly and has a sort of "skirt" making it
hard to digest; it is more frequent on the open seas where the intensity
of upwelling decreases.

[Drawing: Jordi Corbera, from data provided by the author]

44 Vertical distribution of trypton (seston that is not plankton)
in average dry weight, in the oceanic waters off western and
northwestern Australia, according to observations by A. Hagmeier (summer
1961), on a logarithmic scale. The suspended material consists of
non-living particles, about which there is very little information, as
well as live plankton.

[Drawing: Editronica, based on several sources]

45 The marine laboratory at Rosgo (Roscoff) at the beginning of the
20th century. This marine laboratory on the Brittany coast of the
English Channel was the first of those created by Henry Lacaze-Duthiers
(1821-1901) as coastal extensions to his zoology laboratory at the
Sorbonne. Although its founder was most interested in marine
invertebrates, since its beginnings the Roscoff laboratory has
contributed to many aspects of marine biology, especially the plankton
of the Channel and the neighboring Atlantic.

[Photo: Station Biologique de Roscoff]

46 Arctic and Antarctic waters are characterized by spectacular
phytoplankton blooms during their summers, as shown by these false color
satellite images (warm tones indicate high photosynthetic activity).
Phy-toplankton blooms are due to the availability of light, which is
limited or absent during the winter. Note the difference between the
Arctic and the Antarctic (left and right respectively) as the Arctic is
surrounded by land, while the Antarctic is a sea surrounding a
continent.

47 Model of the formation of eddies and grids of descending water
surrounding small eddies of rising deep water in the northern
hemisphere. The force of the wind generates horizontal movements that,
when compounded by the Earth's rotation, give rise to alternating
eddies in opposite directions. Anticyclonic eddies (clockwise in
northern hemisphere and anticlockwise in the south) tend to stratify
lighter water at their center and to expand until they fuse laterally
with others. Cyclonic eddies (in the opposite directions) suck up deep
water in their center, bringing nutrient-rich water to the illuminated
surface, and thus show greater fertility, but they tend to become
narrower and maintain themselves separated from the grid structure
created by the anticyclonic eddies.

[Drawing: Jordi Corbera, using data provided by the author]

48 The strong absorption of light by water is even apparent in
transparent water, as shown here in the center of the Pacific, close to
the Hawaiian islands. A jellyfish Cephea cephea is moving against a blue
background clearly showing the transparency of the nutrient-poor water.
This absorption of light is one of the most rigorously conditioning
factors of phytoplankton, which progressively loses its source of energy
as it settles until it reaches a depth where it is insufficient for
photosynthesis.

[Photo: David B. Fleetham / Natural Science Photos]

49 Comparison of production and presence of silicon dioxide on the
surface of sediments in the Pacific and Indian Oceans, and a generalized
model of the accumulation of sediments on the seafloor. The production
of silicon oxides by phytoplankton (mainly by diatoms and to a lesser
extent by silicoflagellates and radiolarians, which are more common in
tropical waters) is expressed in grams of silicon per square meter per
year, while that of amorphous silicon (opal) as a percentage of dry
weight of carbonate-free sediment. The maximum values for concentrations
of amorphous silicon in sediment are found between the Antarctic
convergence and the Antarctic divergence, but slightly displaced from
the zones of maximum production. Relative production maxima are found
that can be related to areas of upwelling and divergence in these oceans
and that are also reflected in the sediments of the equatorial band of
the eastern Pacific. In a generalized model of oceanic sedimentation,
siliceous muds would tend to accumulate in areas of upwelling of the
eastern shores of the ocean and under the equatorial divergences, while
in the centers of the hemi-oceans red clays, poor in organic materials,
would accumulate, reflecting their scarce productivity.

[Drawing: Editronica, based on data from Lisitzin]

50 The struggle against settling out of the sunlit zone is a
priority for phytoplankton organisms. Those that develop the most
successful strategies, such as the large extensions that increase the
buoyancy of the diatom Chaetoceros, are usually the species responsible
for plankton blooms when conditions allow.

[Photo: Claude Carre / Jacana]

51 Representation of the main characteristics of the phytoplankton
(plankton "mandalas") using different descriptors. The first
uses as descriptors turbulence and presence of nutrients. The upper
right box corresponds to the beginning of succession, while the lower
left box corresponds to its end. The start typically shows considerable
turbulence and persistence of nutrients in the sunlit layers (as well as
being dominated by opportunistic species with high rates of
reproduction). The end of succession is characterized by low turbulence
and nutrient depletion (and is dominated by specialized, persistent
species with low rates of reproduction). The bottom right box would
correspond to very turbulent spring waters in a Nordic or Antarctic sea,
almost without nutrients and organisms (the Gran-Braarud effect). The
upper left box shows the situation in bays or other stratified waters
near the coasts where the surface water receives additional nutrients,
often of continental origin: In these situations swimming
dinoflagellates (often toxic) bloom and accumulate, causing "red
tides." The same diagram can be rotated by 45[degrees] (clockwise)
to change the coordinates that become, respectively, the quotient of
nutrients divided by turbulence and the product of nutrients multiplied
by turbulence, which now correspond to stratification and productivity,
respectively. The axis of succession (and of change in dominant
reproductive strategies) now runs from right to left.

[Diagram: Jordi Corbera, using data provided by the author]

52 A colony of polyps, in the form of a planktonic medusa, of
Porpita porpita. This is the most common form of the species, and is an
asexual phase. This colony consists of a central polyp specialized in
feeding (the gastrozooid), above which there is a circular floater.
Around the gastrozooid there are polyps specialized in reproduction
(gonozooids), and between them at the type of the umbel, are circles of
polyps specialized in defense (dactylozooids), arm-ed with many
cnidoblasts borne in small spheres that may completely cover the
specimen. Their color is due to the presence of symbiotic zooxanthellae
that nourish the polyps. The medusa phase is the shortest and smallest
phase in the life cycle of this species. It is only 2 mm wide, while the
polyp colony can reach a diameter of 10 mm.

[Photo: Peter Parks / Norbert Wu Photography]

53 The biological cycle of many zooplankton species is very
complicated. The copepod Acartia clausi from the Atlantic coast of the
Americas is an example. The drawing shows the different stages of its
life cycle, its length, percentage survival, and the number of
individuals that survive each stage out of the total that hatched
initially. The complete cycle may last up to 14 days, but the cycle of
the population as a whole is longer, as the adult females have a life
expectancy of five days. While they are in the plankton, if enough food
is available, the females can lay eggs several times. In the species A.
tonsa, when food concentration is 100 g of carbon per liter, 46% of its
energy goes into growth, 33% into reproduction, and the other 21% is
lost by excretion. If food is increased 4-fold, feeding increases
3.5-fold, and the energy invested in reproduction is doubled. But if
food is increased 9-fold, assimilation increases only a little, and
reproductive effort hardly increases.

[Drawing: Jordi Corbera, from several sources]

54 The dispersal and distribution of many zooplankton organisms are
intimately linked to the dynamics of water masses. An example of this
phenomenon is the dispersal of the larvae of the anchovy Engraulis
capensis in the southeast Atlantic. The adults lay their eggs near Cape
Agulhas, where the water column is mixed and not very productive. The
eggs hatch within a few days, forming lecithotrophic larvae (ones that
feed on their yolk) that are able to feed within a week. After a month,
they are 20 mm long, and when they 60-70 mm they are juveniles. The
larvae drift to the north in a strong current that bears them more than
149 mi (240 km) to a highly productive upwelling above Cape Colombine,
thus ensuring an abundant food supply. The adults return to the region
of Cape Agulhas the following southern spring or summer to spawn.

[Drawing: Jordi Corbera, from several sources]

55 Phases in the development of the medusa Pelagia noctiluca, which
forms large masses, or swarms. They do this, among other reasons, so
that their eggs can form new medusae directly and do not have to pass
through a benthic polyp stage like other species. The ciliated,
elongated, free-swimming larva (planula larva of P. noctiluca) has a
darker end where the mouth forms (upper left). A few days later, the
larva flattens and forms the rough fissured rim (upper center and right)
that will make it a true medusa. Next, it becomes a new larval form, the
ephyra, the first indication that it will form a large swarm, and it is
often found in large quantities in samples of plankton (center right).
The larvae take three months to complete development to the adult
medusa, during which time they remain in the same water mass and so
they, too, can form dense populations that may drift to the coast on
surface currents.

56 Shrimp larvae are a good example of what plankton organisms have
to do to avoid sinking. Many species develop a range of morphological
structures, such as body projections and filamentous appendages, which
give them a neutral buoyancy and, as a result, they do not have to
expend energy to move and avoid sinking in the water column.

[Photo: Peter Parks / Norbert Wu Photography]

57 Planktonic pteropods (sea butterflies), such as this individual
of the genus Creseis, may be herbivorous or carnivorous. The shells of
herbivorous pteropods are very thin and almost transparent. The
herbivores browse on phytoplankton or filter it from a large volume of
water, which they draw to their mouth by the constant movement of the
cephalo-bucal prolongations that emerge from their shells.

[Photo: Peter Parks / NHPA]

58 Sexual phase of the anthomedusan Neoturris pileata, showing the
red gonads adhered to its stomach. Like most other anthomedusans, it has
a benthic polyp phase whose life is much shorter than the adult's.
The tentacles around the umbrella of this widely distributed species of
anthomedusa may reach three times the length of the body, which is about
1 or 2 in (3 or 4 cm). This species is carnivorous, catching small prey
such as copepods.

[Photo: Claude Carre]

59 Euchaeta marina is a widely distributed copepod of tropical,
subtropical and temperate waters, where it forms dense populations in
the top 328 ft (100 m). It can migrate strongly and avoids the surface
water during the hours of light. It is also clearly seasonally
distributed with peaks of abundance in spring and winter, but it
disappears almost completely from the plankton during the summer.

[Photo: Claude Carre]

60 Calanus finmarchicus is one of the largest calanoid copepods,
with adults up to 4 mm long. It is very abundant in the North Atlantic,
where it forms dense swarms close to the coasts. The life expectancy of
an adult female is two and a half months, although the population
generated at the beginning of summer lives for seven months, until the
onset of winter. The males remain in the plankton for a shorter period
than the females. Like other species of zooplankton, C. finmarchicus
performs ontogenetically distinct migrations. The females clearly
migrate to the surface at night, while the males stay a few meters below
it. The nauplius and smaller copepodid larvae do not perform vertical
migrations.

[Photo: Robert Arnold / Planet Earth Pictures]

61 Many benthic organisms have a pelagic larval stage, lasting from
a few days to several months. The echinoderms, such as Amphiura
filiformis, have several larval stages, one of which, the ophiopluteus,
is very abundant in the coastal plankton for a few weeks. The different
larvae undergo a process of morphological transformation until they
reach a stage similar to that of the adult, when recruitment takes
place. Larval mortality is very high and up to 95% of each brood is
lost.

[Photo: Claude Carre]

62 Chaetognaths are planktonic organisms that are very common at
certain periods of the year.They are highly seasonal. The species of the
genus Sagitta form dense populations in the meso-and epipelagic waters
at varying times of the year, while at other times they may be almost
absent. It is not clear if their eggs are present in a latent state, or
if there are so few individuals that they are not captured by plankton
nets. Chaetognaths are carnivorous animals and frequently, cannibals.

[Photo: Peter Parks / NHPA]

63 Ostracods are among the smallest organisms of the zooplankton.
They are especially abundant in mid-latitude surface waters and can be
caught in neustonic nets. Although there are many benthic species, the
planktonic species are more diverse and show wide horizontal and
vertical ranges. They are active filter-feeders that can form dense
populations at certain times of the year, when they play an important
role in coastal planktonic communities.

[Photo: Claude Carre]

64 Nanomia bijuga is a colony of siphonophores consisting of polyps
with differing morphology and functions.

The colony can reach 7 ft (2 m) in length, although the nectophores
are at most 3 mm long. The upper part of the colony consists of buoyant
nectophores, underneath the pneumatophore responsible for the
colony's vertical orientation and buoyancy. The cluster of
nectophores responsible for buoyancy produces a long stolon on which the
other polyps are located. The most visible polyps are the gastrozooids
(responsible for feeding), the gonozooids (reproductive), and the
tentacles, which are specialized and highly retractile polyps. The
colony captures its prey by extending its long tentacles in a volume of
water greater than 5 cubic yards (4 cubic meters), forming a type of
very fine net that is invisible to the occasional passing prey that
adhere to it.

[Photo: Claude Carre]

65 Interspecific associations are much more common in the
zooplankton than might be expected of organisms that live in a dilute
environment like a body of water. One example of an association exists
between medusae (like the Antarctic species Scarcia princeps, shown in
the photo) and hyperiid amphipods. The association generally starts as
commensalism, with the amphipod eating part of the medusa's prey,
and it may turn into parasitism, because the amphipod eats the medusa if
other prey is not available. This type of association often starts with
the implantation of eggs in the medusa's mesogloea by an adult
female amphipod. When the embryos hatch, their larval development takes
place within the medusa, which they feed upon. The senescence of the
host means that once they are adults the amphipods have to find another
host to settle on and to lay their eggs on.

[Photo: Norbert Wu / Still Photography]

66 The underside (ventral) of pelagic fish is often lighter in
color than the upper side (dorsal), as shown by this stingray (Dasyatis
americana). This combination, together with the reflections and hues of
the water itself, make the fish less visible from above (against the
dark ocean depths) and from below (against the light).

[Photo: Norbert Wu / Still Photography]

67 Predation is intense in the pelagic environment, and is
practiced by members of most animal groups. The photo shows a sparid
fish caught by a coelenterate and about to be ingested.

[Photo: Peter Parks / Norbert Wu Still Photography]

68 The migrations of some species of pelagic fish. In one way or
another, most pelagic fish migrate large distances. The term
oceanodromous is used for species that migrate within the oceans.
Diadromous refers to fish that migrate between fresh and salt waters.
The map shows the migration routes of four oceanodromous fish: the
herring (Clupea arengus), the cod (Gadus morhua), the tuna (Thunnus
thynnus) and the skipjack tuna (Euthynnus pelamis). It also shows two
groups of diadromous fish: the eels and the salmons. Both European eels
(Anguilla anguilla) and American eels (A. rostrata) are catadromous,
reproducing in the sea and feeding and growing in freshwater. Both the
Atlantic salmon (Salmo) and the Pacific salmon (Oncorhynchus) are
anadromous--feeding and growing in the sea and reproduce in freshwater.

[Drawing: Editronica, from several sources]

69 Annual production cy-cles in different oceanic regions. Annual
cycles of primary and secondary production are more seasonal at polar
latitudes. At high Arctic or Antarctic latitudes there is a single peak
of primary production in the summer, followed by a peak of secondary
production, also in the summer but slightly out of phase. At
mid-latitudes there are two peaks of primary production (the most
important is in the spring, the autumn one is secondary) and one peak in
the summer of secondary production by herbivores. At equatorial
latitudes there are no seasonal peaks, only slight oscillations within
the tendency of primary producers (algae) and herbivores to maintain
uniform production throughout the year.

[Drawing: Editronica, based on data from Cushing, 1959]

70 Mass of engraulids (Anchoa) in the Pacific, near the Galapagos
Islands. One of the engraulids' most remarkable characteristics is
that they live in large schools that move as a single unit, and this
makes their exploitation especially attractive to humans. However, their
populations may vary greatly in very short periods, and this is favored
by their excessive exploitation in some of the places where they are
most abundant, such as the coasts of Peru and northern Chile.

[Photo: D. Parer & E. Parer-Cook / Auscape International]

71 Simplified diagram of food webs in the Antarctic Ocean, probably
one of the most complex seas, with the longest food chains in the entire
pelagic environment. To make it simpler, some details are not included:
Some cephalopods eat small fish and are thus tertiary consumers, seals
and birds export some of their production from the marine environment,
and the great skua (Stercorarius skua) migrates from pole to pole,
leaving the southern hemisphere to breed.

[Diagram: Editronica, from various sources]

72 Clupeids, like engrau-lids, form very large schools. Both can
eat phytoplankton thanks to their cellulase-producing intestinal
bacterial symbionts. This allows clupeids, like this shoal of herrings
(Clupea harengus), to grow fast and reach high levels of biomass that
are food for larger predators, including humans.

[Photo: Norbert Wu Photography]

73 Carangids (saurels, jacks, trevally, and similar) are
middle-sized pelagic fish, although some are almost the same size and
show the same gregarious behavior as small phytoplankton-eating fish.
Carangids do not eat phytoplankton, but feed on zooplankton and the
juvenile forms of other fish or marine organisms. The photo shows a
school in the Turks and Caicos Islands, in the Antilles.

[Photo: Yves Lefevre / Bios / Still Pictures]

74 Typical circular school of barracudas (Sphyraena), a large (up
to 7 ft [2 m]) predatory fish with ferocious teeth, frequent in all
tropical seas. The juveniles in particular form large groups that swim
in circles. They do not form groups as large as some smaller fish.

[Photo: Norbert Wu Photo-graphy]

75 Cephalopods are voracious predators and also the favorite prey
of some large fish, especially the predatory cetaceans. They vary
greatly in size, from squid and cuttlefish a few centimeters long, such
as this Indonesian coral shield squid (Sepioteuthis lessoniana), to the
49 ft (15 m) long giant deep sea squid, the favorite food of the sperm
whale (see insert, "Whale food," page 98).

[Photo: David B. Fleetham / Natural Science Photos]

76 Bonitos (Sarda) are powerful swimmers that migrate long
distances. The scombrids have an unusual physiology and are the only
warm-blooded fish.

[Photo: Juan Carlos Calvin]

77 Marine mammals are present throughout the Earth's seas.
They have adapted their physiology to the marine environment. The right
whale (Eubalena glacialis, above) prefers to live in warm waters and
approaches the coast to reproduce; they usually feed by swimming close
to the surface with their mouth open, filtering with their baleen
plates. Dolphins, such as the pan-tropical species Stenella longirostris
(below) are among the most abundant marine mammals, especially in highly
productive areas. They eat small- and medium-sized fish and cephalopods.

78 Migratory routes of some marine birds. Although all marine birds
nest on land and many remain within a relatively restricted territory,
others migrate over thousands of kilometers, from their nesting sites to
their overwintering areas. The Arctic tern (Sterna paradisaea), the
shearwaters (Puffinus), and the skuas (Stercorarius) migrate almost from
pole to pole. Others, such as Wilson's petrel (Oceanites
oceanicus), only migrate from the temperate areas of one hemisphere to
those of the other. Other migratory birds, such as the wandering
albatross (Diomedea exulans) and the giant petrel (Macronectes
giganteus), take advantage of the dominant winds to move across the
southern oceans, following the parallels. Gannets (Sula) and brent geese
(Branta bernicla) move along the latitudes within a single hemisphere,
while the Cape gannet (Sula capensis) never crosses the equator.

[Drawing: Editronica, based on several sources]

79 Cormorants (Phalacro-corax) and other diving birds actively
exploit the marine environment, especially up-wellings. They remove some
nutrients from the sea, and these accumulate on the cliffs and coastal
islands where the birds nest and reproduce, such as this island in the
Channel Islands National Park, California.

[Photos: Frans Lanting / Bruce Coleman Limited]

80 Turtles of the world. The adult loggerhead turtle (Caretta
caretta) measures between 38 and 45 in (96 and 114 cm) and lives in the
tropical zones of all the oceans, feeding on mollusks and crabs. The
Pacific green turtle (Chelonia agassizii) lives off the coast of Mexico,
Peru and Galapagos Islands; it eats algae and the adults measure 28-36
in (71-91 cm). Not all zoologists separate the green turtles into two
species. The flatback turtle (Chelonia depressa) lives off the north of
Australia and eats holothurians and other invertebrates, and can reach
35 in (90 cm) in length. The leatherback turtle (Dermo-chelys coriacea)
reproduces in the tropics but can also be found in temperate and even
subarctic waters; it eats medusae and attains the largest size of any
marine reptile, 60-70 in (152-178 cm). The Kemp's ridley
(Lepidochelys kempi) is found in the Gulf of Mexico and the north
Atlantic; it eats crabs and mollusks and reaches 23-26 in (58-66 cm).
The hawksbill turtle (Eretmochelys imbricata), whose carapace (shell) is
of great decorative value, lives in tropical oceans close to coral or
rocky reefs and measures from 11-14 in (28-36 cm). The green turtle
(Chelonia mydas), lives in all the tropical oceans, except the east
Pacific; it eats algae and marine plants and measures 35-43 in (90-110
cm). The Pacific Ridley (Lepi-dochelys olivacea) lives in the tropical
oceans, mainly the east Pacific, the Indian, and the south Atlantic; it
eats crustaceans, fish eggs, and vegetation. It may reach a length of
23-26 in (58-66 cm).

[Drawing: Anna Maria Ferrer]

* The classification used in this work is based on the division of
living beings into five kingdoms (see volume 1, p. 75), proposed by
Robert H. Whittaker in 1959, according to which most phytoplankton
organisms are protoctists, and not members of the plant kingdom
(although the term suggests they are plants). The term phytoplankton is
still a valid designation for planktonic primary producers in spite of
the taxonomic inexactitude implied by its etymological meaning of
"plant plankton." The same is true for zooplankton, or
"animal plankton," which also includes many protoctists.

** The 1989 Handbook of Protoctists, by L. Margulis, J.O. Corlyss,
M. Melkonian, and D.J. Chapman, considers the Dinoflagellata or
Dinomastigota as an independent phylum of protoctists.

*** The 1989 Handbook of Protoctists, by L. Margulis, J.O. Corlyss,
M. Melkonian, and D.J. Chapman includes the prasinophytes within the
chlorophytes, and considers them to be the phylogenetic origin of the
chlorophytes.

**** The 1989 Handbook of Protoctists, by L. Margulis, J.O.
Corlyss, M. Melkonian, and D.J. Chapman considers the haptophytes or
prymnesiophytes, and diatoms or Bacillariophyta as two independent types
of protoctists, and includes the silicoflagellates as a class within the
Chrysophyta (also considered as a separate phylum), called the
Dictyochophyceae.

***** The 1989 Handbook of Protoctists, by L. Margulis, J.O.
Corlyss, M. Melkonian, and D.J. Chapman includes the prasinophytes
within the chlorophytes, and considers them to be the phylogenetic
origin of the chlorophytes.

****** This work considers the Euglenida as a separate phylum of
protoctists.

******* This work considers the Raphidophyta as a separate phylum
of protoctists, although some authors consider it a class of
Chlorophyta.

******** Zooplankton species exist that are carnivorous and thus
secondary consumers, but this term is reserved for the larger marine
predators (large crustaceans, fish, etc.).

COPYRIGHT 2000 COPYRIGHT 2009 Enciclopedia Catalana, SAU
No portion of this article can be reproduced without the express written permission from the copyright holder.